Traits of recalcitrant seeds in a semi-deciduous tropical forest in Panamá: some ecological implications


  • M. I. DAWS,

    Corresponding author
    1. Seed Conservation Department, Royal Botanic Gardens Kew, Wakehurst Place, Ardingly, West Sussex RH17 6TN, and
      †Author to whom correspondence should be addressed. E-mail:
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  • N. C. GARWOOD,

    1. Department of Botany, Natural History Museum, Cromwell Road, London SW7 5BD, UK
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    • §

      Present address: Department of Plant Biology, Southern Illinois University, Carbondale, IL 62901-6509, USA


    1. Seed Conservation Department, Royal Botanic Gardens Kew, Wakehurst Place, Ardingly, West Sussex RH17 6TN, and
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†Author to whom correspondence should be addressed. E-mail:


  • 1We used cross-species and phylogenetic analyses to compare seed traits of 36 species with desiccation-sensitive and 189 with desiccation-tolerant seeds from a semi-deciduous forest in Panamá.
  • 2When correcting for phylogenetic dependence between taxa, the desiccation-sensitive seeds were significantly larger than desiccation-tolerant seeds (3383 vs 283 mg) and typically shed during the wet (as opposed to dry) season. Both traits presumably reduce the rate of seed drying and hence the risk of desiccation-induced mortality for the desiccation-sensitive species.
  • 3Growing-house germination trials in simulated understorey and canopy gap environments revealed that the desiccation-sensitive species germinated most rapidly. Additionally, on a proportion basis, the desiccation-sensitive seeds allocated significantly less resources to seed physical defences (endocarp and/or testa) which may partially facilitate rapid germination. Both relationships were significant when correcting for phylogenetic dependence and seed mass.
  • 4Our results suggest that, for large-seeded species which will dry slowly, desiccation sensitivity may be advantageous. Rapid germination may reduce the duration of seed exposure to predation, and the low investment in physical defence means that, per unit mass, desiccation-sensitive seeds are a more efficient use of resources in seed provisioning.


Based on their response to desiccation, seeds can be divided into two broad categories: orthodox and recalcitrant. Orthodox (hereafter termed desiccation-tolerant) seeds can be dried to low water contents (<7%) with little effect on viability (Roberts 1973). In contrast, recalcitrant (hereafter termed desiccation-sensitive) seeds are killed by drying to water contents as high as 20–30% (Pritchard 2004). Because desiccation-sensitive seeds progress towards germination when stored wet, they are difficult to store for anything other than the short term. Thus their use in reforestation and ex situ conservation programmes is problematic.

A range of studies have attempted to predict seed responses to desiccation from seed, plant and habitat variables (Tompsett 1984, 1987; Hong & Ellis 1997, 1998; Dickie & Pritchard 2002; Pritchard et al. 2004). Desiccation-sensitive seeds have been reported to be, on average, larger than desiccation-tolerant seeds, a feature that will reduce the rate of seed drying. For example, Dickie & Pritchard (2002) reported the mean seed mass of 205 desiccation-sensitive tree and shrub species to be 3958 mg compared with 329 mg for 839 desiccation-tolerant species. However, a potential problem with this analysis is that it treats species as independent when, in fact, closely related species share evolutionary history and therefore are not independent. This can result in spurious significances if a suite of closely related species share some unrelated traits (Harvey & Pagel 2000). Instead, branching events in the phylogenetic tree involving a change in seed storage behaviour, and the associated change in seed mass (or other traits), should be identified and used as independent data points. Only a single study appears to have investigated whether seed mass is associated with desiccation tolerance while correcting for phylogenetic dependence between taxa (Gleiser et al. 2004). This study compared the seed mass of just two desiccation-sensitive and 22 desiccation-tolerant Acer species and reported that the desiccation-sensitive species had larger seeds. However, as this study included only two desiccation-sensitive species, one of which has recently been re-evaluated and found to be desiccation-tolerant, this conclusion is tentative (Daws et al., in press).

In a study of 886 tree and shrub species, Tweddle et al. (2003) reported that desiccation-sensitive seeds are most common in tropical rainforests, where they contribute ≈47% of species and are infrequent in drier environments such as savanna (≈12% of species). Even within dry environments, species with desiccation-sensitive seeds can minimize the risk of seed desiccation by timing seed shed to the period of maximum rainfall (Pritchard et al. 2004). An alternative strategy has been reported for nine species in the genus Coffea, where the level of desiccation tolerance is related to the duration of the dry period after seed shed: species shed before a prolonged dry spell were more desiccation-tolerant than those shed prior to a short dry spell (Dussert et al. 2000).

It has been suggested that desiccation tolerance is the ancestral state in seeds and has subsequently been lost in species with desiccation-sensitive seeds (Farnsworth 2000; Oliver, Tuba & Mishler 2000; Dickie & Pritchard 2002). The ability to tolerate desiccation is clearly advantageous, and enables seed persistence both through time and in relatively arid environments (Pammenter & Berjak 2000). While having large, round seeds shed to coincide with the peak in annual rainfall may minimize the risk of desiccation for desiccation-sensitive seeds, it is not yet clear whether seed desiccation sensitivity is a neutral trait, or whether there are selection benefits associated with desiccation sensitivity (Pammenter & Berjak 2000).

One potential advantage of seed desiccation sensitivity may be rapid germination. Desiccation-sensitive seeds are shed at high water contents, are metabolically active, and in some cases are actively progressing towards germination (Berjak et al. 1984). Consequently, limited or no imbibition is required for germination to progress rapidly following dispersal. This proposition has been tested for a limited number of African dryland trees by Pritchard et al. (2004) who found that, at a constant temperature of 25 °C, three taxa with desiccation-sensitive seeds germinated more rapidly than six desiccation-tolerant taxa.

Mast fruiting and rapid germination of dipterocarp seeds (Curran & Webb 2000), the vast majority of which are desiccation-sensitive (Tompsett & Kemp 1996), is thought to result from selection pressure from vertebrate seed predators. Similarly, Pammenter & Berjak (2000) have proposed that for climax species in tropical forests, many of which have desiccation-sensitive seeds, the formation of a seedling bank will reduce seed predation by fungi. Consequently, rapid germination of desiccation-sensitive seeds may minimize both the risk of seed drying and the duration of exposure to predation. Consequently there may be reduced selection for investing resources in seed physical defences, in terms of both reducing predation risk and the mechanical restraint to germination. In the study by Pritchard et al. (2004), an average of 15% of the dispersal unit was endocarp/testa for three desiccation-sensitive species compared with 46% for seven desiccation-tolerant species. Pritchard et al. (2004) hypothesized that desiccation-tolerant species require greater defences because dispersal may occur in the dry season or during short dry spells, and seeds may be exposed to predation in the soil seed bank for extended periods. However, the wider applicability of the findings of Pritchard et al. (2004) is unclear, particularly given the small data set involved (10 species).

Seed mass can vary over 10 orders of magnitude, and for tropical tree seeds may be correlated with germination rate: for 179 Malaysian tree species Foster (1986) reported a significant positive correlation between seed mass and time to first germination. Seed mass may also be positively related to the proportion of seed resources allocated to physical defences (e.g. within a family; Fenner 1983; Schütz 2000). Consequently, to address more fully the implications of desiccation sensitivity for seed mass, germination rates and seed defences, analyses that account for phylogenetic relationships and/or seed mass are also required.

In this paper we examine these propositions for a data set of 225 tree and shrub taxa from a semi-deciduous tropical forest in Central Panamá, including 36 with desiccation-sensitive seeds. Specifically, we use cross-species analyses and account for phylogenetic relationships to address the following questions: (1) Are desiccation-sensitive seeds larger than desiccation-tolerant seeds? (2) Do desiccation-sensitive seeds germinate more rapidly than desiccation-tolerant seeds, and does this relationship hold when accounting for seed mass? (3) Do desiccation-sensitive seeds have a lesser investment in physical defences than desiccation-tolerant seeds, and is this true when accounting for seed mass? In addition, using cross-species analyses we test whether desiccation-sensitive seeds are dispersed when water is most available (when the risk of drying is minimal), while desiccation-tolerant seeds may be shed in wet or dry periods. The results are discussed in the context of the ecological costs/benefits of seed desiccation sensitivity.

Materials and methods

study site and species

This study was conducted on the Barro Colorado Nature Monument (BCNM), Republic of Panamá (9°10′ N, 79°51′ W). Vegetation on the BCNM consists of semi-deciduous tropical forest, and has been described in detail elsewhere (Leigh, Rand & Windsor 1982): nomenclature follows the Flora of Panama Checklist (D’Arcy 1987). Rainfall on the BCNM averages 2600 mm year−1, with a pronounced dry season between January and April (Dietrich, Windsor & Dunne 1982).

Ripe fruits/seeds, at the point of natural dispersal, were collected from 226 tree, liana and shrub species (see Appendix 1) between 1985 and 1989. Fleshy fruits were cleaned by removing the fleshy pulp within 2 days of collection: no cleaning was necessary for wind-dispersed seeds and those in dry, dehiscent pods. For each species the month of seed collection was recorded and seed dry mass was determined by drying c. 10 cleaned seeds per species (with fruit tissue removed) at 60 °C for 3 days.

Data on seed desiccation tolerance was collated from Release 6 of the Royal Botanic Gardens Kew's online Seed Information Database (SID; Flynn, Turner & Dickie 2004). Seed responses to desiccation are divided into three categories in SID: orthodox (desiccation-tolerant); recalcitrant (desiccation-sensitive); and intermediate. Intermediate seeds have seed storage characteristics that are intermediate between those of orthodox and recalcitrant taxa and account for only ≈2% of SID. Species in the data set were assigned to these seed storage categories, resulting in 189 orthodox, 36 recalcitrant and 0 intermediate taxa.

germination experiments

Where seed numbers allowed, germination tests were conducted on each seed collection within the growing house in the laboratory clearing on Barro Colorado Island (BCI; part of the BCNM). Following collection, seeds were stored at 25 °C and sown within 2 days. For germination experiments, seeds were sown in plastic or fibre (peat) pots containing unsterilized soil collected from within the forest. The number of seeds sown per pot was determined primarily by seed size, and ranged from one per pot in the case of the larger-seeded species (e.g. Prioria copaifera) to 200 for the smallest seeded species (e.g. Conostegia spp.). For each species between 20 and 200 seeds were planted. Seeds were sown on the soil surface in an attempt to mimic natural dispersal by wind, being dropped by animals or deposited in faeces. However, a few of the larger-seeded species are actively buried by scatter-hoarding rodents; we did not take this into account. As a number of the species in this study can be classified as pioneers (sensuSwaine & Whitmore 1988) and require high-light conditions for germination (Daws et al. 2002a), pots were split between the upper and lower shelves in the growing house to mimic conditions within canopy gaps (upper shelf) and closed understorey sites (lower shelf) (Garwood 1983; Molofsky & Augspurger 1992). On the upper shelf, irradiance levels averaged 18·5 ± 0·7% (±1 SE) full sunlight vs 2·3 ± 0·2% on the lower shelf. These values are typical of medium-sized gaps and intact understorey sites, respectively, on BCI (Daws et al. 2002a; Pearson et al. 2002).

Pots were watered daily or as required (Garwood 1983), and germination was scored at weekly intervals until either (1) all seeds had germinated; (2) all remaining seeds were badly damaged or had disappeared from the pots (restricted to larger-seeded species); or (3) >3 months had passed with no further germination since the last germination event. Consequently, many germination tests extended up to 3 years. Germination was scored as visible seedling emergence.

For each taxa, the mean time to germination (MTG) on both upper and lower shelves of the growing house was calculated using the following equation:

MTG = Σ (n × d)/N( eqn 1 )

where n is the number of seeds germinated between scoring intervals; d the incubation period in days at that time point; and N the total number of seeds germinated in the treatment (Tompsett & Pritchard 1998).

Determination of resource allocation to defence

For each species, a minimum of eight individual seeds (dispersal unit) were dissected into their component parts: endocarp/testa and embryo/endosperm. These component parts were subsequently dried at 103 °C for 17 h (ISTA 2004) followed by mass determinations. To calculate the allocation to defence (seed-coat ratio, SCR), the ratio of the mass of covering structures (endocarp and testa) to the mass of the total dispersal unit was determined (Grubb & Burslem 1998; Pritchard et al. 2004).

statistical analysis

One-way anova implemented in minitab 13 (Minitab Inc., State College, PA, USA) was used to test for a relationship between desiccation sensitivity and seed mass, MTG or SCR. In all analyses, seed mass was logarithmically and SCR arc-sine transformed to ensure homoscedasticity. For both cross-species and phylogenetic analyses involving MTG, two separate analyses were performed using MTG in the shade (MTGS; lower shelf) and in the light (MTGL; upper shelf). MTG was transformed using a Box–Cox transformation with the optimum value of λ determined using minitab 13. This resulted in λ values of −0·224 and −0·225 for MTGS and MTGL, respectively. The effect of either MTG or SCR on desiccation sensitivity while removing the effect of seed mass was tested using ancova in minitab 13. In addition, sign tests were used to test the null hypothesis, for desiccation-sensitive and desiccation-tolerant species separately, of no difference between MTG in light and in shade.

For each species the timing of dispersal was classified as dry or wet season. This classification was based on whether dispersal occurred in January to April, inclusive (dry season) or May to December (wet season) (Daws et al. 2005). Subsequently, for desiccation-tolerant and desiccation-sensitive species, a χ2 test of association was used to test the null hypothesis of no association between response to drying and timing of dispersal.

Phylogenetically independent contrasts (Felsenstein 1985; Pagel 1992) were used to analyse the relationship between desiccation sensitivity and seed mass, MTG and SCR. This approach is based on the logic of comparing pairs of species within a phylogeny that share an immediate common ancestor. The null hypothesis is that there is no correlation between changes in traits at the nodes. The package caic (Purvis & Rambaut 1995) was used to generate contrasts. Within the phylogeny we assumed that all branch lengths were the same: analyses of simulated data sets suggest that equal branch lengths may perform better than estimated branch lengths (Purvis, Gittleman & Luh 1994). For these analyses, the Brunch procedure, designed for discrete predictor variables, was used (Purvis & Rambaut 1995).

For analyses testing whether the transition from desiccation-tolerant to desiccation-sensitive seeds is associated with changes in either MTG or SCR while holding the effect of seed mass constant, contrasts between mass and MTG or SCR were calculated using the Crunch procedure in caic, designed for continuous data (Purvis & Rambaut 1995). Subsequently a linear regression, forced through the origin, was fitted to the contrasts. A linear regression with the same slope was then fitted to the raw data for mass and MTG and for mass and SCR, and the contrasts from the line recorded. Changes in these contrasts associated with seed desiccation tolerance were subsequently analysed using the Brunch procedure. All contrasts were analysed using a sign test (Purvis & Rambaut 1995). In all phylogenetic analyses, the latest phylogeny available to (sub-) family level from the Angiosperm Phylogeny Group was used (APG II 2003). However, due to the wide range of families and the lack of complete phylogenies to genus level for many families, a series of polytomies were created. Exceptions (classification source given in parentheses) were the Anacardiaceae (Aguilar-Ortigoza & Sosa 2004), Arecaceae (Uhl & Dransfield 1987), Clusiaceae (Gustafsson, Bittrich & Stevens 2002), Fabaceae (Polhill 1994), Lauraceae (Li et al. 2004), and Meliaceae (Muellner et al. 2003).


seed mass and seed-coat ratio

Taxa with desiccation-sensitive seeds had a significantly greater seed mass than taxa with desiccation-tolerant seeds (3383 vs 283 mg, P < 0·05; Table 1, Fig. 1). When correcting for phylogenetic relatedness, this relationship was still significant (P < 0·05; Table 1), indicating that the transition from desiccation-tolerant to desiccation-sensitive seeds is significantly correlated with an increase in seed mass.

Table 1.  Results of statistical analyses investigating the effect of desiccation tolerance/sensitivity on the relationship between seed mass, seed-coat ratio and mean time to germination in shade (MTGS) or light (MTGL)
Independent variableCovariate–Phylogeny +Phylogeny  
dfF+ve contrasts–ve contrasts
  1. Analyses either assumed that species were statistically independent data points (–phylogeny), or accounted for phylogenetic relatedness between species (+phylogeny).

  2. ns, Not significant; *, P < 0·05; **, P < 0·01; ***, P < 0·001.

Seed mass1, 21268·6***19 1**
Seed coat ratio1, 10638·5*** 217**
Seed coat ratioSeed mass1, 10128·0*** 413*
MTGS1, 19410·8** 315*
MTGSSeed mass1, 19311·0*** 117**
MTGL1, 201 3·6 ns 315*
MTGLSeed mass1, 194 7·3** 117**
Figure 1.

Box plots comparing (a) seed dry mass; (b) mean time to germinate in the shade; and (c) seed-coat ratio for desiccation-sensitive and desiccation-tolerant seeded species. Numbers adjacent to boxes refer to number of species included in the comparison. Boxes span the 25th to 75th percentiles; whiskers span the 5th to 95th percentiles. Dashed and solid lines across boxes show mean and median, respectively.

The SCR for desiccation-sensitive seeds was significantly lower than for desiccation-tolerant seeds (0·212 vs 0·512, P < 0·05; Table 1, Fig. 1): this relationship was still significant when controlling for both effects of seed mass and phylogenetic relationships (P < 0·05; Table 1).

mean time to germination

In the shade treatment, the desiccation-sensitive seeds germinated more rapidly than desiccation-tolerant seeds (MTG 23·3 vs 47·7 days, P < 0·05; Table 1); the relationship was marginally non-significant in the light treatment (P = 0·061; Table 1). Taking into account the effect of seed mass, germination occurred significantly more rapidly for desiccation-sensitive seeds in both light and shade environments (Table 1). In addition, these relationships were phylogenetically robust (Table 1).

The desiccation-sensitive species were significantly more likely to germinate rapidly in the shade than in the higher-light treatment (sign test, 22 species where MTGS < MTGL; three species where MTGS > MTGL, P < 0·001). However, for the desiccation-tolerant species there was no significant bias to either rapid germination in the shade or higher-light treatments (sign test, 86 species where MTGS < MTGL; 84 species where MTGS > MTGL, P > 0·05).

Across species, there was a highly significant (P < 0·001) relationship between MTG and the spread of germination times (difference between the first and last days on which germination occurred) (Spearman's rank correlation, rs = 0·70, df = 194; rs = 0·72, df = 201, for germination in the shade and light, respectively). Thus with an increasing MTG, species had an increasing spread of germination times.

timing of seed dispersal

The distribution of seed dispersal times in relation to the wet and dry seasons was non-random (Table 2; χ2 = 11·0, df = 1, P < 0·001), with desiccation-sensitive seeds more likely to be dispersed in the wet than in the dry season (Fig. 2a). However there were exceptions, such as Virola sebeifera for which seed dispersal occurred at the beginning of the dry season (January; Fig. 2a). In contrast, desiccation-tolerant seeds were more likely to be shed in the dry than in the wet season (Fig. 2b).

Table 2.  Contingency table for observed number of species with desiccation-sensitive and desiccation-tolerant seeds dispersed in either the dry or wet season on Barro Colorado Island
Seed typeTiming of seed dispersal
Dry seasonWet season
  1. Values in parentheses are the expected number of species assuming a 2 × 2 contingency table.

Desiccation-sensitive 5 (13·5)27 (18·5)
Desiccation-tolerant86 (77·5)97 (105·5)
Figure 2.

Frequency distribution of the timing of dispersal for (a) 32 desiccation-sensitive; and (b) 183 desiccation-tolerant species in relation to the wet and dry seasons on Barro Colorado Island. The frequency of dispersal in each month is standardized by the number of species in the comparison. Horizontal lines indicate an even distribution of dispersal throughout the year.


timing of dispersal and seed desiccation sensitivity

For species with desiccation-sensitive seeds, dispersal occurred predominantly in the wet, as opposed to the dry season, with the pattern reversed for desiccation-tolerant species. Similar results have been demonstrated by Pritchard et al. (2004) for African dryland trees, where the desiccation-sensitive species timed seed dispersal to the wettest month(s) of the year, while desiccation-tolerant seeds were dispersed in either wet or dry months. For desiccation-sensitive seeds, wet-season dispersal has the advantage of minimizing the likelihood of seed desiccation and consequent death. However, for desiccation-tolerant seeds, dry-season dispersal has the advantage of allowing a seasonal seed bank to accumulate prior to the onset of significant rains, when the (pre-)existence of a seed bank may facilitate site pre-emption in advance of species without a seed bank (Garwood 1983; Daws et al. 2005). However, there were exceptions among desiccation-sensitive species. For example, V. sebeifera was dispersed primarily early in the dry season (January). Interestingly, the distribution of this species on BCI is significantly biased towards slope sites (Harms et al. 2001), which maintain a higher level of water availability throughout the dry season. On slope sites, even in the dry season, the matric potential at the soil surface rarely falls below levels that are likely to inhibit germination (approximately −1·5 MPa) (Daws et al. 2002a, 2002b). Consequently, the specialization of this species to wet microsites may circumvent selection for wet-season seed dispersal. This reinforces the hypothesis that desiccation-sensitive seeds are shed to coincide with high water availability, albeit in this case related to spatial rather than temporal patterns.

germination and desiccation sensitivity

In our study the desiccation-sensitive species germinated more rapidly than the desiccation-tolerant species, independently of seed mass and phylogeny. This supports our hypothesis that, based on their high water content (which will minimize the period of imbibition) and metabolic activity at dispersal, desiccation-sensitive seeds will germinate rapidly. Although the observed differences in mean germination times between desiccation-sensitive and desiccation-tolerant species (≈38 days) may seem considerable, imbibition in some large, non-hard-seeded species can be protracted. For example, complete imbibition of dry seeds of Hyophorbe lagenicaulis (Arecaceae) has been reported to take 20 days (Wood & Pritchard 2003). Rapid germination of desiccation-sensitive seeds post-dispersal may enable rapid access to soil water, thereby minimizing the risks of desiccation-induced mortality in short wet-season dry spells.

For desiccation-tolerant species, less rapid germination and a greater spread of germination times may be advantageous. For example, in environments of unpredictable rainfall, such as the start of the wet season on BCI (Garwood 1983), less rapid germination, which is dispersed in time, may reduce the risk of drought or desiccation-induced mortality once seeds have either started to germinate or are at the early seedling stage (Doussi & Thanos 2002). However, this may not be a viable strategy for desiccation-sensitive species, for which slow germination and a prolonged dry spell following seed dispersal could potentially result in mortality of an entire annual cohort of seeds.

For 179 Malaysian tree and shrub species, Foster (1986) reported a positive relationship between seed size and germination rate, which was likely to result from reduced seed–soil contact with increasing seed size. However, the relationship between MTG and desiccation sensitivity that we observed was still significant when controlling for seed mass. While the number of desiccation-sensitive species in the data set used by Foster (1986) is unclear, our findings suggest that the high water content of desiccation-sensitive seeds at shedding and their metabolic activity result in rapid germination, irrespective of seed–soil contact.

In a cross-species analysis, the desiccation-sensitive species were more likely to germinate rapidly in the shade than in the light. In higher-light conditions, there may be a negative impact on large-seeded species as a result of water loss and the consequent decrease in vigour associated with desiccation damage (Pammenter & Berjak 2000). In support of this proposition, Molofsky & Augspurger (1992) reported that in gaps on BCI, seeds of the desiccation-sensitive species Gustavia superba (see Appendix 1) germinate to a higher level when buried under leaf litter than when exposed on the soil surface, presumably because of water loss. However, in the shade, litter had no effect on germination. Similarly, burial can have a beneficial effect on the germination and survival of desiccation-sensitive Quercus rubra seeds (Garcia, Banuelos & Houle 2002). These findings highlight the potential importance of burial by seed predators or burial beneath leaf litter for successful establishment of species with desiccation-sensitive seeds. However, the desiccation-tolerant species were equally likely to geminate rapidly in the shade (lower-shelf) or light (upper-shelf) treatments. For the generally small-seeded desiccation-tolerant species, germination in the higher-light environment may be less inhibited as a result of a greater level of seed–soil contact. Additionally, a number of desiccation-tolerant species have been classified as ‘pioneers’ (sensuSwaine & Whitmore 1988), for example Ochroma pyrimidale and Miconia argentea (Pearson et al. 2002). These species rely on the occurrence of open (high-light) microsites for successful germination and seedling establishment, and have seedlings with a physiological requirement for high-light conditions.

seed mass, seed-coat ratio and desiccation sensitivity

Desiccation-sensitive species in this study had large seeds which will presumably reduce the rate of seed desiccation. Interestingly, our values for average seed mass for desiccation-sensitive and desiccation-tolerant species were similar to values presented by Dickie & Pritchard (2002), who included values from a wide range of both tropical and temperate vegetation types. Our observed trend of desiccation-sensitive seeds being large was phylogenetically robust, leading us to suggest that the loss of desiccation tolerance during evolution has been associated with an increase in seed mass. However large seed size per se does not result in desiccation sensitivity. For example, there are a number of large-seeded desiccation-tolerant species in the data set, including Astrocaryum standleyanum and Dipteryx panamensis, both of which have a seed mass >6 g.

In addition to being metabolically active at seed shed, the thin seed coat of desiccation-sensitive species may also contribute to rapid germination by providing less of a mechanical restraint to germination. Our results for MTG and SCR are consistent with the hypothesis of Pritchard et al. (2004) that rapid germination of desiccation-sensitive seeds may reduce the duration of seed exposure to predation (cf. dipterocarps; Curran & Webb 2000), the corollary being reduced selection for a large investment in seed physical defences. Consequently, per unit mass, desiccation-sensitive seeds appear to be a more efficient use of resources in seed provisioning than desiccation-tolerant seeds.

For some groups of species it has been demonstrated that larger seeds may invest proportionally more resources in defence (e.g. Asteraceae; Fenner 1983). However, the differences in SCR we observed were independent of mass. There is also limited evidence for a negative relationship between seed mass and post-dispersal seed predation (Hulme 1998). Viewed in the light of these two relationships, the generally large-seeded desiccation-sensitive species have a surprisingly low investment in physical defences, which presumably reflects the limited time span of seed exposure to predators. Grubb et al. (1998) demonstrated a positive relationship between both seed physical defences and seed nitrate content for a range of tropical tree seeds. Consequently, it is also possible that a low allocation to defence in desiccation-sensitive species may be related to their being of low nutritional value. Investigations into the chemical composition of desiccation-sensitive and desiccation-tolerant species may be worth pursuing to clarify this issue.


There are a number of advantages associated with large seed size, including a higher probability of seedling survival under low light (Leishman & Westoby 1994a) and drought conditions (Leishman & Westoby 1994b), and an ability to resprout following herbivory (Harms & Dalling 1997). However, large and hydrated seeds can be very attractive to both fungal and vertebrate seed predators. In habitats of benign, uniform climate that are continuously conducive to germination and seedling establishment, there may be little selection driving the evolution or maintenance of desiccation tolerance, particularly for large seeds that will dry slowly (Pammenter & Berjak 2000). Our results for germination rate and seed resource allocation support the hypothesis of Pammenter & Berjak (2000) that, in this habitat, desiccation sensitivity may not necessarily be a neutral trait, and may be related to the risk of predation. Thus desiccation sensitivity may be advantageous by minimizing predation through rapid germination, with the consequent low investment in defence resulting in these seeds being a more efficient use of resources in seed provisioning.


We thank Dr Vigdis Vandvik for advice and comments on the manuscript. Hazel Cleland and Justine Hall provided technical assistance at RBG Kew, and the late Eduardo Sierra and Ruth Linklater (née Dempsey) provided most of the assistance in Panamá. Financial support to N.G. was provided by the NSF (BSR-8517395), NERC (GR3-69511) and the Smithsonian Tropical Research Institute. Financial support to M.I.D. and H.W.P. was provided by the Millennium Commission, The Wellcome Trust and Orange plc. The Royal Botanic Gardens, Kew receives grant-aided support from Defra, UK.


Table Appendix 1..  Details of species used in the study: classification to family level [following APG (2003)], seed dry mass, seed-coat ratio, and timing of dispersal relative to wet season (W) and dry season (D) on Barro Colorado Island (species with desiccation-sensitive seeds in bold type)
SpeciesCladeOrderFamilyDWT (mg)Seed- coat ratioDispersal period
Abarema macradenium PittierEurosids IFabalesFabaceae900·153W
Abuta racemosa (Thunb.) Triana & PlanchEudicotsRanunculalesMenispermaceae579 D
Adelia triloba (Müll. Arg.) HemsleEurosids IMalpighialesEuphorbiaceae260·354D
Adenopodia polystachya (L.) J.R. Dixon ex CroatEurosids IFabalesFabaceae2980·942D
Aegiphila elata Sw.Euasterids ILamialesVerbenaceae60 W
Albizia guachapele (H.B. & K.) DugandEurosids IFabalesFabaceae320·433W
Alchornea costaricensis Pax & K. Hoffm.Eurosids IMalpighialesEuphorbiaceae340·799W
Alibertia edulis (Rich.) A. Rich. ex DC.Euasterids IGentianalesRubiaceae150·114D
Alseis blackiana Hemsl.Euasterids IGentianalesRubiaceae0·2 D
Anacardium excelsum (Bertero & Balb. Ex Kunth) SkeelsEurosids IISapindalesAnacardiaceae15070·433D
Andira inermis (Sw.) KunthEurosids IFabalesFabaceae7920·297W
Annona acuminata Saff.MagnoliidsMagnolialesAnnonaceae36 D
Annona glabra L.MagnoliidsMagnolialesAnnonaceae2290·358W
Annona hayesii Saff. In Standl.MagnoliidsMagnolialesAnnonaceae62 W
Annona muricata L.MagnoliidsMagnolialesAnnonaceae3220·706W
Annona purpurea Moç. & Sessé ex DunalMagnoliidsMagnolialesAnnonaceae897 W
Annona spraguei SaffordMagnoliidsMagnolialesAnnonaceae34 W
Anthodon panamense A.C. Sm.Eurosids ICelastralesCelastraceae810·438D
Antirhea trichantha (Griseb.) Hemsl.Euasterids IGentianalesRubiaceae10 W
Apeiba membranacea Spruce ex Benth.Eurosids IIMalvalesMalvaceae690·776W
Apeiba tibourbou Aubl.Eurosids IIMalvalesMalvaceae170·584W
Aristolochia chapmaniana Standl.MagnoliidsPiperalesAristolochiaceae6 W
Arrabidaea candicans (Rich.) DC.Euasterids ILamialesBignoniaceae19 W
Arrabidaea patellifera (Schltdl.) SandwithEuasterids ILamialesBignoniaceae17 D
Artocarpus altilis (Parkinson) FosbergEurosids IRosalesMoraceae5898 W
Aspidosperma cruenta WoodsonEuasterids IGentianalesApocynaceae565 W
Aspidosperma megalocarpon Müll. ArgEuasterids IGentianalesApocynaceae  D
Astrocaryum standleyanum L.H. BaileyCommelinidsArecalesArecaceae7598 W
Astronium graveolens Jacq.Eurosids IISapindalesAnacardiaceae300·368D
Bactris gasipaes KunthCommelinidsArecalesArecaceae16800·303W
Beilschmiedia pendula (Sw.) Hemsl.MagnoliidsLauralesLauraceae39870·100W
Bertiera guianensis Aubl.Euasterids IGentianalesRubiaceae1 W
Bixa orellana L.Eurosids IIMalvalesBixaceae25 D
Brosimum alicastrum Sw.Eurosids IRosalesMoraceae7120·045W
Bursera simaruba (L.) Sarg.Eurosids IISapindalesBurseraceae82 D
Byrsonima spicata (Cav.) KunthEurosids IMalpighialesMalphigiaceae1080·953W
Callichlamys latifolia (Rich.) K. Schum.Euasterids ILamialesBignoniaceae1340·328D
Calophyllum longifolium Willd.Eurosids IMalpighialesClusiaceae45320·266D
Capparis flexuosa L.Eurosids IIBrassicalesBrassicaceae  W
Capparis frondosa Jacq.Eurosids IIBrassicalesBrassicaceae970·262W
Capsicum annuum L.Euasterids ISolanalesSolanaceae3 D
Carica papaya L.Eurosids IIBrassicalesCaricaceae120·459W
Casearia sylvestris Sw.Eurosids IMalpighialesSalicaceae1 D
Castilla elastica SesséEurosids IRosalesMoraceae  W
Cavanillesia platanifolia (Bonpl. in Humb. & Bonpl.) KunthEurosids IIMalvalesMalvaceae1751 D
Cecropia insignis Liebm.Eurosids IRosalesMoraceae0·5 D
Cecropia longipes PittierEurosids IRosalesMoraceae0·7 W
Cecropia obtusifolia Bertol.Eurosids IRosalesMoraceae0·50·878W
Cecropia peltata L.Eurosids IRosalesMoraceae0·6 D
Cedrela odorata L.Eurosids IISapindalesMeliaceae11 W
Ceiba pentandra (L.) Gaertn.Eurosids IIMalvalesMalvaceae550·309D
Celtis iguanaea (Jacq.) Sarq.Eurosids IRosalesCeltidaceae106 W
Cespedezia macrophylla Seem.Eurosids IMalpighialesOchnaceae0·2 D
Chamaedorea tepejilote Liebm.CommelinidsArecalesArecaceae1500·053W
Chloroleucon mangense (Jacq.) J.F. Macbr.Eurosids IFabalesFabaceae45 W
Chromolaena odorata (L.) R.M. King & H. Rob.Euasterid IIAsteralesAsteraceae0·2 D
Chrysophyllum cainito L.AsteridsEricalesSapotaceae2100·562D
Cissus sicyoides L.Rosids Vitaceae22 D
Citrus aurantfolia L.Eurosids IISapindalesRutaceae  W
Clidemia capitella var. neglecta (D. Don) L.O. WilliamsRosidsMyrtalesMelastomataceae0·02 W
Clidemia capitellata (Bonpl.) D. DonRosidsMyrtalesMelastomataceae  D
Clidemia dentata D. DonRosidsMyrtalesMelastomataceae0·02 W
Clidemia octona (Bonpl.) L.O. WilliamsRosidsMyrtalesMelastomataceae0·010·250W
Clidemia septuplinervia Coqn.RosidsMyrtalesMelastomataceae0·02 W
Clitoria javitensis var. portobellensis (Beurl.) FantzEurosids IFabalesFabaceae483 D
Cochlospermum vitifolium (willd.) Sprenq.Eurosids IIMalvalesCochlospermaceae260·741D
Connarus panamensisEurosids IOxalidalesConnaraceae294 W
Connarus turczaninowii Triana & Planch.Eurosids IOxalidalesConnaraceae4050·214W
Conostegia cinnamomea (Beurl.) Wurdack.RosidsMyrtalesMelastomataceae  W
Conostegia speciosa NaudinRosidsMyrtalesMelastomataceae0·1 W
Cordia alliodora (Ruiz & Pav.) OkenEuasterids I Boraginaceae6 W
Cordia panamensis L. RileyEuasterids I Boraginaceae590·720W
Cordia spinescens L.Euasterids I Boraginaceae11 D
Couroupita guianensis Aubl.AsteridsEricalesLecythidaceae5 D
Coussapoa asperifolia ssp. magnolifolia (Trécul) Akkermans & C.C. Berq.Eurosids IRosalesMoraceae2 D
Coutarea hexandra (Jacq.) K. SchumEuasterids IGentianalesRubiaceae5 D
Crotalaria cajanifolia KunthEurosids IFabalesFabaceae13 D
Cupania cinerea Poepp.Eurosids IISapindalesSapindaceae5100·254W
Cydista aequinoctalis (L.) Miers.Euasterids ILamialesBignoniaceae1120·547D
Dalbergia retusa Hamsl.Eurosids IFabalesFabaceae1300·792D
Dalechampia tiliifolia Lam.Eurosids IMalpighialesEuphorbiaceae21 D
Davilla aspera (Aubl.) BenoistCore Eudicots Dilleniaceae240·337W
Dendropanax arboreus (L.) Decne. & Planch.Euasterid IIApialesAraliaceae80·790W
Desmoncus isthmius L.H. BaileyCommelinidsArecalesArecaceae3140·261W
Didymopanax morototoni (Aubl.)Euasterid IIApialesAraliaceae140·642D
Dioclea guianensis Benth.Eurosids IFabalesFabaceae72 D
Dioclea reflexa Hook. f.Eurosids IFabalesFabaceae40130·672W
Dipteryx panamensis (Pittier) Record & mellEurosids IFabalesFabaceae61270·870D
Elaeis oleifera (Kunth) CortésCommelinidsArecalesArecaceae25070·694W
Enterolobium cyclocarpum (Jacq.) Griseb.Eurosids IFabalesFabaceae5450·470W
Erythrina costaricensis MicheliEurosids IFabalesFabaceae  W
Eugenia uniflora L.RosidsMyrtalesMyrtaceae 0·141 
Ficus citrifolia Mill.Eurosids IRosalesMoraceae0·9 W
Ficus dugandii Standl.Eurosids IRosalesMoraceae0·1 W
Ficus insipida Willd.Eurosids IRosalesMoraceae1 W
Ficus obtusifolia KunthEurosids IRosalesMoraceae10·635W
Ficus popenoei Standl.Eurosids IRosalesMoraceae0·5 W
Garcinia mangostana L.Eurosids IMalpighialesClusiaceae7480·281W
Genipa americana L.Euasterids IGentianalesRubiaceae123 W
Guarea guidonia (L.) SleumerEurosids IISapindalesMeliaceae1530·267W
Guazuma ulmifolia Lam.Eurosids IIMalvalesMalvaceae40·488D
Gustavia superba (Kunth.) O. Berq.AsteridsEricalesLecythidaceae28150·061W
Hamelia patens Jacq.Euasterids IGentianalesRubiaceae0·05 W
Hampea appendiculata (Donn. Sm.) Standl.Eurosids IIMalvalesMalvaceae600·187D
Henriettea succosa (Aubl.) DC.RosidsMyrtalesMelastomataceae0·09 W
Henriettella fasicularis TrianaRosidsMyrtalesMelastomataceae0·02 W
Herrania purpurea (Pittier) R.E. SchultEurosids IIMalvalesMalvaceae2170·296D
Hevea brasiliense Müll. ArgEurosids IMalpighialesEuphorbiaceae36300·525W
Hippobroma longiflora (L.) G. DonEuasterids IIAsteralesCampanulaceae0·07 W
Hura crepitans L.Eurosids IMalpighialesEuphorbiaceae8450·327W
Hybanthus prunifolius (Humb. & Bonpl. Ex Roem. & Schult.) Schulze-MenzEurosids IMalpighialesViolaceae120·268W
Hyeronima laxiflora (Tul.) Müll. ArgEurosids IMalpighialesEuphorbiaceae70·699D
Hylenaea praecelsa (Miers) A.C. Sm.Eurosids ICelastralesCelastraceae20270·670D
Hymenaea courbaril L.Eurosids IFabalesFabaceae5418 D
Inga minutula (Schery) T.S. Elias.Eurosids IFabalesFabaceae3800·141W
Inga punctata Willd.Eurosids IFabalesFabaceae  W
Jacaranda copaia (Aubl.) D. Don.Euasterids ILamialesBignoniaceae5 W
Laetia procera (Poepp.) EichlerEurosids IMalpighialesSalicaceae50·762D
Lafoensia punicifolia DC.RosidsMyrtalesLythraceae360·516D
Lantana camara L.Euasterids ILamialesVerbenaceae9 W
Leandra dichotoma (D. Don) Coqn.RosidsMyrtalesMelastomataceae0·008 W
Lonchocarpus pentaphyllus (Poir.) KunthEurosids IFabalesFabaceae1610·156W
Luehea seemannii Triana & Planch.Eurosids IIMalvalesMalvaceae30·784D
Macfadyena unguis-cati (L.) A.H. GentryEuasterids ILamialesBignoniaceae290·633D
Mangifera indica L.Eurosids IISapindalesAnacardiaceae45000·381W
Margaritaria nobilis L.f.Eurosids IMalpighialesEuphorbiaceae80·756W
Maripa panamensis Hemsl.Euasterids ISolanalesConvolvulaceae3530·094W
Melochia lupulina Sw.Eurosids IIMalvalesMalvaceae0·3 D
Melothria trilobata Coqn. In Mart.Eurosids ICucurbitalesCucurbitaceae4 W
Merremia umbellata (L.) Hallier f.Euasterids ISolanalesConvolvulaceae35 D
Mesechites trifida (Jacq.) Müll. Arg.Euasterids IGentianalesApocynaceae30·429W
Miconia affinis DC.RosidsMyrtalesMelastomataceae0·2 W
Miconia argentea (Sw.) DC.RosidsMyrtalesMelastomataceae0·080·274D
Mikania micrantha KunthEuasterid IIAsteralesAsteraceae0·09 D
Mimosa pigra L.Eurosids IFabalesFabaceae16 W
Mouriri myrtilloides ssp. parvifolia (Benth.) MorleyRosidsMyrtalesMelastomataceae680·116W
Muntingia calabura L.Eurosids IoxalidalesElaeocarpaceae0·04 D
Myroxylon balsamum (L.) HarmsEurosids IFabalesFabaceae478 W
Nectandra membranacea (Sw.) Griseb.MagnoliidsLauralesLauraceae 0·159 
Ochroma pyramidale (Cav. Ex Lam.) Urb.Eurosids IIMalvalesMalvaceae100·940D
Ocotea whitei WoodsonMagnoliidsLauralesLauraceae73000·013W
Odonellia hirtiflora (M. Martens & Galeotti) K.R. RoberstonEuasterids ISolanalesConvolvulaceae27 D
Odontadenia macrantha (Roem. & Schutt.) Markgr.Euasterids IGentianalesApocynaceae1720·379D
Ormosia coccinea (Aubl.) JacksonEurosids IFabalesFabaceae543 W
Ormosia macrocalyx DuckeEurosids IFabalesFabaceae4010·131W
Ossaea quinquenervia (Mill.) Coqn.RosidsMyrtalesMelastomataceae0·010·207W
Pachira aquatica Aubl.Eurosids IIMalvalesMalvaceae1730 D
Pachira quinata (Jacq.) DugandEurosids IIMalvalesMalvaceae40 D
Pachira sessilis (Bentham) Pittier.Eurosids IIMalvalesMalvaceae3490·206D
Pachyrhizus erosus (L.) Urb.Eurosids IFabalesFabaceae763 D
Palicourea guianensis Aubl.Euasterids IGentianalesRubiaceae14 W
Passiflora ambigua Hemsl.Eurosids IMalpighialesPassifloraceae34 D
Passiflora biflora Lam.Eurosids IMalpighialesPassifloraceae3 W
Passiflora foetida L.Eurosids IMalpighialesPassifloraceae80·650D
Persea americana Mill.MagnoliidsLauralesLauraceae206700·037W
Petrea aspera Turcz.Euasterids ILamialesVerbenaceae35 D
Phryganocydia corymbosa (Vent.) Baill.Euasterids ILamialesBignoniaceae69 D
Piper aequale VahlMagoliidsPiperalesPiperaceae0·06 W
Piper dilatatum Rich.MagoliidsPiperalesPiperaceae0·1 W
Piper hispidum Sw.MagoliidsPiperalesPiperaceae0·1  
Piper marginatum Jacq.MagoliidsPiperalesPiperaceae0·10·208D
Piper peltatum L.MagnoliidsPiperalesPiperaceae0·040·147W
Pithecoctenium crucigerum (L.) A.H. GentryEuasterids ILamialesBignoniaceae59 D
Platymiscium pinnatum (Jacq.) DugandEurosids IFabalesFabaceae3130·791D
Platypodium elegans VogelEurosids IFabalesFabaceae12190·892D
Pleonotoma variabilis (Jacq.) MiersEuasterids ILamialesBignoniaceae32 D
Poulsenia armata (Miq.) Standl.Eurosids IRosalesMoraceae65 W
Pouteria sapota (Jacq.) H.E. Moore & StearnAsteridsEricalesSapotaceae130400·472W
Prionostemma aspera (Lam.) MiersEurosids ICelastralesCelastraceae1820·431D
Prioria copaifera Griseb.Eurosids IFabalesFabaceae238400·366W
Protium panamense (Rose) I.M. Johnst.Eurosids IISapindalesBurseraceae48000·256W
Protium tenuifolium ssp. sessiliflorum (Rose) D.M. PorterEurosids IISapindalesBurseraceae1300 W
Pseudobombax septenatum (Jacq.) DugandEurosids IIMalvalesMalvaceae600·246D
Psidium guajava L.RosidsMyrtalesMyrtaceae80·861W
Psychotria acuminata Benth.Euasterids IGentianalesRubiaceae12 W
Psychotria brachybotrya Müll. Arq.Euasterids IGentianalesRubiaceae4 W
Psychotria deflexa DC.Euasterids IGentianalesRubiaceae4 W
Psychotria horizontalis Sw.Euasterids IGentianalesRubiaceae6 W
Psychotria micrantha Kunth.Euasterids IGentianalesRubiaceae100·575W
Psychotria pittieri Standl.Euasterids IGentianalesRubiaceae3 W
Psychotria pubescens Sw.Euasterids IGentianalesRubiaceae8 W
Psychotria tomentosa (Aubl.) VahlEuasterids IGentianalesRubiaceae9 W
Quararibea pterocalyx Hemsl.Eurosids IIMalvalesMalvaceae40400·356W
Randia formosa (Jacq.) Schum.Euasterids IGentianalesRubiaceae310·523W
Rheedia edulis (Seem.) Planch.Eurosids IMalpighialesClusiaceae2890·252W
Rhynchosia pyramidalis (Lam.) Urb.Eurosids IFabalesFabaceae61  
Roupala montana Aubl.EudicotsProtealesProteaceae19 D
Serjania decapleuria CroatEurosids IISapindalesSalindaceae48 D
Serjania rhombea Radlk.Eurosids IISapindalesSapindaceae110·829D
Simarouba amara Aubl.Eurosids IISapindalesSimaroubaceae105 W
Siparuna guianensis Aubl.MagnoliidsLauralesMonimiaceae200·618W
Solanum hayesii FernaldEuasterids ISolanalesSolanaceae20·807D
Solanum torvum Sw.Euasterids ISolanalesSolanaceae1 W
Souroubea sympetala GilgAsteridsEricalesMarcgraviaceae3 D
Spondias mombin L.Eurosids IISapindalesAnacardiaceae 0·957 
Stizolobium pruriens (L. in Stickm.) Medik.Eurosids IFabalesFabaceae5290·176D
Stylogyne standleyi LundellAsteridsEricalesMyrsinaceae660·278D
Swartzia simplex var. ochnacea (Sw.) Sprenq.Eurosids IFabalesFabaceae10250·048W
Swietenia macrophylla KingEurosids IISapindalesMeliaceae4700·290D
Symphonia globulifera L.f.Eurosids IMalpighialesClusiaceae2334 D
Synechanthus warscewiczianus H. Wendl.CommelinidsArecalesArecaceae2720·105W
Syzygium jambos L.RosidsMyrtalesMyrtaceae23800·076 
Tabebuia guayacan (Seem.) Hemsl.Euasterids ILamialesBignoniaceae260·204D
Tabebuia rosea (Bertol.) DC.Euasterids ILamialesBignoniaceae25 D
Tachigali versicolor Standl. & L.O. WilliamsEurosids IFabalesFabaceae9100·275W
Terminalia amazonia (J.F. Gmel.) ExellRosidsMyrtalesCombretaceae2 D
Terminalia oblonga (Ruiz & Pav.) Steud.RosidsMyrtalesCombretaceae55  
Tetracera portobellensis Bewl.Core Eudicots Dilleniaceae14 D
Tetrathylacium johansenii Standl.Eurosids IMalpighialesSalicaceae1 D
Theobroma cacao L.Eurosids IIMalvalesMalvaceae17710·275 
Tournefortia hirsutissima L.Euasterids I Boraginaceae2 W
Trema micrantha (L.) BlumeEurosids IRosalesUlmaceae20·682W
Trichilia tuberculata C. DC.Eurosids IISapindalesMeliaceae1510·038W
Trichospermum galeottii (Turcz.) Kosterm.Eurosids IIMalvalesMalvaceae30·571D
Triplaris cumingiana Fisch. & C.A. Mey. ex C.A. MeyCore EudicotsCaryophyllalesPolygonaceae83 D
Triumfetta bogotensis DC.Eurosids IIMalvalesMalvaceae22 D
Vernonia patens KunthEuasterid IIAsteralesAsteraceae0·1 D
Virola sebifera Aubl.MagnoliidsMagnolialesMyristiceae4720·223D
Virola surinamensis (Rol.) Warb.MagnoliidsMagnolialesMyristiceae19520·103W
Vismia macrophylla KunthEurosids IMalpighialesClusiaceae0·6 W
Vochysia ferruginea Mart.RosidsMyrtalesVochysiaceae  W
Zanthoxylum belizense LundellEurosids IISapindalesRutaceae14 D
Zanthoxylum panamense P. WilsonEurosids IISapindalesRutaceae290·791D
Zanthoxylum procerum Don. Sm.Eurosids IISapindalesRutaceae11 W
Zanthoxylum setulosum P. WilsonEurosids IISapindalesRutaceae10 W