Dispersal potential and early growth in 14 tropical mangroves: do early life history traits correlate with patterns of adult distribution?

Authors


Peter J. Clarke, Botany, The University of New England, Armidale 2351, Australia (e-mailpclarke1@metz.une.edu.au).

Summary

  • 1We characterized the dispersal potential and early growth traits of 14 tropical mangrove species in experiments where diaspores were immersed in various solutions of seawater and subsequently stranded onto surfaces with the same salinity.
  • 2Viviparous and non-viviparous species had similar buoyancy, seed weight and rates of root and shoot initiation, as well as early growth and salinity tolerance. This trait convergence may be related to selection against small, dormant diaspores in the unstable regeneration niche.
  • 3Differences in dispersal potential and early growth of 12 species were compared with known patterns of distribution (across the shore, along estuaries, regional occurrence and continental range size) to test if tidal sorting of diaspores could account for adult spatial patterns.
  • 4Diaspore buoyancy, orientation, lateral root initiation, shoot initiation and early shoot extension differed among species but none correlated with adult zonation across the shore or along estuaries. However, some back-shore species had diaspores that were buoyant and were slow to initiate lateral roots and shoots. Patterns of early growth were partially related to the distribution along estuaries but salinity responses contributed to this zonation in only three species.
  • 5Regional distributions were unrelated to dispersal potential. However, the tendency of infrequent species to show slow growth in full seawater may account for the under-saturation of species in estuaries with appropriate habitats. The range size of the tropical mangroves appears unrelated to their dispersal potential and early growth traits.
  • 6Early life history traits of 12 mangroves showed poor correlation with patterns of adult distribution across all spatial scales. Traits related to establishment were, however, stronger predictors of distribution than those associated with dispersal.

Introduction

Dispersal and early growth are plant life history stages that fundamentally determine where species grow and in what abundance in mangrove systems. Differences in diaspore (seeds, fruits and seedlings) dispersal potential and early growth traits may help explain pronounced stand patterns ranging in scale from shore-parallel zonation of species (101–102 m), to estuary zonation of species (102–104 m), to between estuary (regional) variation in species distribution (104–106 m) (Tomlinson 1986; Duke 1992).

Ecological sorting at early life-history stages (regeneration niche models) may lead to the habitat differentiation or ‘zonation’ commonly observed in mature stands of mangroves (Rabinowitz 1978a; Smith 1987; Clarke & Allaway 1993; McKee 1995; McGuinness 1997). The tidal sorting of diaspores (Rabinowitz 1978a,b,c; Tamai & Iampa 1988; Jimenez & Sauter 1991) has largely been replaced as an explanation by the sorting of species along a salinity gradient as a result of competitive interactions (Ball 1988) or due to the interactions of multiple variables (for example Smith 1987; Smith et al. 1989; Osborne & Smith 1990). More recently the combined effects of sorting due to dispersal and early growth have been used to explain small-scale patterns of recruitment (McGuinness 1997; Minchinton 2001) and zonation (Clarke 1995; McKee 1995).

Many regeneration niche models have been tested using elaborate manipulative field experiments in which diaspores are stranded in early growth sites to which experimental treatments (disturbance, predators, competitors, etc.) are applied. Dispersal potential may, however, influence the behaviours of these diaspores and thus interpretation of field experiments involving diaspore transplants (McKee 1995). Tidal action may not deliver diaspores of all species to all sections of the intertidal zone (cf. Smith 1992) and tidal sorting of diaspores in relation to dispersal ability, as emphasized by Rabinowitz (1978a,b), may need revisiting. Initial factors that may influence the distribution and fate of diaspores include dispersal potential (weight, shape, orientation, time to shoot emergence, and buoyancy of diaspores) and early growth (time and numbers of plants with initiated roots and shoots), as these traits interact with the environments where dispersal and stranding occur.

In addition to the potential effects of tidal sorting on shore-parallel zonation, it may affect distribution of species along estuary tidal and salinity gradients (see Duke 1992), although this has rarely been examined (Smith 1992). In part this was due to the lack of comprehensive quantitative information about regional patterns of species along estuaries, which for tropical mangroves have only recently been published (Bunt 1996). These data show that mangrove species often have distributions along estuary gradients that are consistent with general accounts (for example Chapman 1976; Tomlinson 1986; Duke 1992) and may be related to salinity (for example Bunt et al. 1982; Duke 1992), although the cause remains speculative (Smith 1992).

Surveys in northern Australia (Wells 1995; Bunt 1996; Ball 1998) have also revealed patterns of species distribution between estuaries and enable species to be ranked in order of their relative frequency within the absolute bounds of their geographical distribution. These surveys suggest that habitats (estuaries) were under-saturated with mangrove species, possibly because some species are unable to disperse and establish from supply populations. Furthermore, the variable range size of mangrove species (Tomlinson 1986) is well documented for species in northern Australia (Duke 1992). Several hypotheses have been advanced for these geographical ranges (Tomlinson 1986; Duke 1992) but the potential effects of dispersal potential and early growth have not been tested.

The aim of our study was to compare the early life history traits (dispersal potential and early growth) of tropical mangroves with adult distributions at four scales: (i) shore parallel zonation, (ii) estuary or river zonation, (iii) frequency of species occurrence among estuaries and (iv) geographical range around a coastline. We also examined whether diaspore characteristics of weight, size and dispersal potential are correlated with early growth traits in mangroves, and whether viviparous and non-viviparous mangrove species have different dispersal and early growth abilities.

Materials and methods

Diaspore buoyancy, orientation and root initiation

Diaspores from 14 tropical species of mangroves (Table 1) were subjected to immersion in different salinity treatments at the Australian Institute of Marine Science, Townsville. Nomenclature follows Tomlinson (1986) and Duke (1992), with the exception of the reclassification of Ceriops tagal var. australis as C. australis by Ballment et al. (1988). None are known to be dispersed other than in water, but a range of plant families and germination types was included (Table 1). Diaspores were generally collected by picking mature fruit from trees to prevent exposure to the osmotic effects of tidal water once they had fallen. However, Heritiera littoralis and Cynometra iripa were only available by collecting dry intact fruits recently deposited underneath parent trees and Ceriops australis had to be collected from the strandline, but this species was excluded from correlative analyses due to potentially confounding effects of pre-exposure to tidal water. The fresh weights of all diaspores were recorded within 3 days of collection. All diaspores were collected from mangrove stands (Lucinda and Cape Cleveland) within 100 km of Townsville, Australia (19°17′ S, 147°03′ E).

Table 1.  Germination type and seed and seedling characteristics of mangrove species used in experiments. Vivipary, germination descriptions and propagule type are from Tomlinson 1986. Nomenclature for Avicennia from Duke 1992
SpeciesFamilyViviparyPropagule typeGerminationPropagule elongationPropagule curvatureGrowth form
Aegialitis annulataPlumbaginaceaeCryptoviviparousSeedEpigealElongatedCurvedShrub
Aegiceras corniculatumMyrsinaceaeCryptoviviparousOne-seeded fruitEpigealElongatedCurvedShrub
Avicennia marina var.  eucalyptifoliaAvicenniaceaeCryptoviviparousOne-seeded fruitEpigealNot elongatedTree
Bruguiera exaristataRhizophoraceaeViviparousSeedlingEpigealElongatedStraightTree
Bruguiera gymnorrhizaRhizophoraceaeViviparousSeedlingEpigealElongatedStraightTree
Bruguiera parvifloraRhizophoraceaeViviparousSeedlingEpigealElongatedCurvedTree
Ceriops australisRhizophoraceaeViviparousSeedlingEpigealElongatedStraightTree
Ceriops decandraRhizophoraceaeViviparousSeedlingEpigealElongatedStraightTree
Ceriops tagalRhizophoraceaeViviparousSeedlingEpigealElongatedStraightTree
Cynometra iripaLeguminosaeNoneOne-seeded fruitEpigealNot elongatedShrub
Heritiera littoralisSterculiaceaeNoneOne-seeded fruitHypogealNot elongatedTree
Lumnitzera racemosaCombretaceaeNoneOne-seeded fruitEpigealNot elongatedTree
Rhizophora stylosaRhizophoraceaeViviparousSeedlingEpigealElongatedStraightTree
Xylocarpus mekongensisMeliaceaeNoneSeedHypogealNot elongatedTree

Four salinity treatments were used (100%, 50%, 10% and 0% seawater) in polythene storage bins (60 L). For each species, treatment was replicated three times with a total of five diaspores per bin. The bins each contained a single species and were arranged in a randomized block in a shade house where they were stirred by hand each day and replenished with water if evaporation reduced water levels. Buoyancy, orientation and initiation of root or shoot primordia were recorded after 1, 2, 3, 5, 10 and 15 days.

The time taken for species to develop roots (the ‘obligate dispersal period’, Rabinowitz 1978a) corresponds with the period where diaspores are not able to derive resources from sediments. Note that, in the cases where vivipary or cryptovivipary results in the elongation of the hypocotyl, the obligate dispersal period is the time taken for development of ‘lateral’ roots, not the emergence of the radicle. These diaspores were added to solutions and the time taken for lateral roots to emerge (1 mm long) was measured, together with numbers of roots.

The effects of salinity on the number of diaspores floating, and the number of diaspores developing roots, or lateral roots from hypocotyls, were analysed for each species with a single factor anova. Cochran’s test was used to test for homogeneity of variances, no transformations were required. The correlations among continuous diaspore variables were also calculated.

Post-dispersal initiation of shoots

At the end of the immersion experiment, stranding was simulated by transferring five diaspores of each species to each of three replicate trays per salinity treatment (70 × 50 cm). Trays were filled with 5 cm of beach sand and saturated with seawater of the same strengths as used for the immersion experiments. We thus avoided problems of osmotic shock that can occur by planting seedlings into saline substrates. Salinities were randomly allocated to trays arranged in blocks. Diaspores were kept in a shadehouse under ambient summer temperatures and moistened to maintain salinity levels. During a period of 15 weeks, survival, sprouting of shoots (elongation to 2 mm) and heights of seedling apical shoots were recorded.

The effects of salinity on the root development and sprouting of each species after 15 weeks were analysed with a single factor anova. Cochran’s test was used to test for homogeneity of variances and ln(x + 1) transformations were applied where necessary.

Population effects

Differences in buoyancy characteristics among populations were assessed for diaspores of A. corniculatum (Lucinda, Townsville, Coffs Harbour 30°18′ S, 153°08′ E), A. marina var. eucalyptifolia (Townsville), A. marina var. marina (Brisbane 27°28′ S, 153°01′ E, Coffs Harbour), B. exaristata (Lucinda, Townsville) and R. stylosa. (Townsville, Brisbane, Coffs Harbour). Forty diaspores per population were collected from several trees and distributed between containers filled with either 100%, 50%, 10% or 0% seawater under similar conditions to those used for the more comprehensive study. The effect of salinity and population on the number of diaspores floating after 15 days was analysed for each species with a two-way anova.

Diaspore trait correlations

We tested for correlations between diaspore traits, i.e. buoyancy (rank order), time to initiate roots (rank order), mean diaspore weight, mean diaspore length, mean proportion of diaspores initiating roots (across all treatments), mean proportion of diaspores initiating shoots (across all treatments). No attempt was made to correlate these traits with other life history traits or to adjust comparisons for phylogeny. Spearman rank correlations were calculated where rank variables were used, otherwise Pearson correlation coefficients were calculated. C. australis and L. racemosa were excluded from the analyses.

Comparison of diaspore attributes with distribution patterns

Quantitative zonation patterns described by Bunt (1996) could not be correlated with diaspore data because of the variable and inconsistent species zonation. Generalized, qualitative positions in intertidal zones were derived from tables presented in Duke (1992) and from descriptions in Tomlinson (1986), providing they were consistent with the results of Bunt (1996). These data were qualitatively compared with the outcome of the trait analysis.

The occurrence of mangrove species in downstream, middle, and upstream locations of estuaries of north-east Queensland (Bunt 1996) was used in correlations of frequency in different tidal positions with diaspore attributes of: buoyancy (rank order), dormancy (time to radicle emergence), weight, % root initiation, % shoot initiation and early growth. Data from systematic surveys of two sets of independent estuaries in northern Australia, a wetter coast in Queensland (Bunt 1996) and a seasonally arid coast in the Northern Territory (Wells 1995), were also used to calculate the relative occurrence of mangrove species within each region. These data were then correlated with diaspore attributes of: buoyancy, dormancy (time to radicle emergence), weight, % root initiation, % shoot initiation and early growth. Note that the term ‘dormancy’ is used in the broadest sense to infer a resting or dispersal phase of the life cycle. In viviparous mangroves, development is often continuous and there is no strict dormancy. Nevertheless, there are differences in the time taken for shoots to emerge (the apparent ‘dormant’ phase).

Finally, measures of the range of species along the coastline of Australia were used to correlate geographical range with diaspore attributes of: buoyancy, dormancy, weight, % root initiation, % shoot initiation and early growth. Data were obtained from Tomlinson (1986), Wells (1995) and our own field observations. Spearman rank correlations were calculated where rank variables were used, otherwise Pearson correlation coefficients were calculated. C. australis was excluded from all analyses and L. racemosa, which remained dormant, was excluded from the analyses where shoot and root initiation were involved.

Results

Diaspore buoyancy, orientation and root initiation

Diaspore characteristics are summarized in Table 2. The buoyancy patterns of the diaspores ranged from obligate floaters to those that sink (Fig. 1, Table 2). All species with elongated straight propagules (Table 1) floated and orientated the dispersal unit to a vertical position, whereas the three species with curved propagules remained in a prone position and sank during the experiments (Table 2). The timing of root initiation ranged from 4 days to more than 3 weeks and the proportion of propagules initiating roots was highly variable within and between species (Table 2). Patterns of root initiation among species appear unrelated to buoyancy and propagule orientation.

Table 2.  Mangrove diaspore attributes of mass, length, buoyancy, immersion orientation, dormancy and root initiation
SpeciesMean fresh mass of propagules (g) (SE)Mean length of propagules (cm)Predominant buoyancy pattern in saltwaterPredominant buoyancy pattern freshwaterPredominant orientation of propagulesTime until root initiation (days)% of propagules with roots at 23 days (SE)
  1. SE = standard error. *Ceriops australis was collected from dispersed propagules and this may confound comparisons. Avicennia marina initially sinks but then refloats. ‡Averaged over all salinity treatments.

Aegialitis annulata 0.25 (0.01) 3SinkerSinkerProne10 18.3 (8.7)
Aegiceras corniculatum 0.51 (0.01) 4SinkerSinkerProne 8 38.0 (19.8)
Avicennia marina var. eucalyptifolia 5.16 (0.14) 3FloaterFloater**Prone 4100.0 (0.0)
Bruguiera exaristata 4.30 (0.15) 9FloaterFloaterProne to vertical 8 70.7 (7.2)
Bruguiera gymnorrhiza24.96 (0.97)18FloaterSinkerVertical14 68.7 (6.3)
Bruguiera parviflora 2.53 (0.05)21SinkerSinkerProne 8 86.7 (6.9)
Ceriops australis* 1.60 (0.03)13FloaterFloaterVertical 8 23.3 (7.3)
Ceriops decandra 2.74 (0.06)15FloaterFloaterProne to vertical 8 58.3 (10.9)
Ceriops tagal 4.65 (0.09)19FloaterFloaterProne to vertical14 8.3 (3.3)
Cynometra iripa 6.72 (0.19) 2FloaterFloaterProne23 3.3 (3.0)
Heritiera littoralis20.93 (1.08) 5FloaterFloaterProne23 8.3 (3.5)
Lumnitzera racemosa 0.17 (0.01) 1SinkerSinkerProneDid not develop 0
Rhizophora stylosa35.37 (1.09)23FloaterFloaterProne to vertical14 3.3 (2.2)
Xylocarpus mekongensis24.49 (0.79) 6FloaterFloaterProne 4 98.3 (11.3)
Figure 1.

Proportion of diaspores floating in tanks of 100%, 50%, 10% and 0% seawater. Mean values shown from five diaspores placed in each of three replicate tanks. Species arranged in order of response from floaters to sinkers.

Salinity treatments had differential effects on buoyancy in some species (Fig. 1c–j) and these were mostly related to the physical effects of denser solutions, i.e. greater buoyancy in full seawater. Species with variable buoyancy were defined as ‘floaters’ if more than 50% of diaspores remained buoyant after 15 days of enforced ‘dispersal’. Interactive effects between salinity and time suggested biochemical changes in diaspores in relation to the surrounding medium, as in Avicennia marina which initially sank but then refloated. Three broad groups of species emerged: (i) those with diaspores that are buoyant and float for the period observed, (ii) those that sink within 5 days of release, and (iii) those where buoyancy changes through time and/or with salinity (Fig. 1, Table 2).

Diaspores of A. marina, C. tagal, C. iripa, H. littoralis, R. stylosa and X. mekongensis tended to float irrespective of salinity treatments. The curved diaspores of A. corniculatum, A. annulata and B. parviflora sank over time in all solutions, whereas buoyancy of L. racemosa, B. gymnorrhiza, B. exarista and C. decandra varied with the density of the solution. L. racemosa was considered a sinker (50–80% of diaspores sink within 15 days) and B. exaristata a floater (73–100% remain buoyant), while B. gymnorrhiza and C. decandra have more varied patterns but generally float in seawater. Correlations between diaspore traits (Table 3) show that weight and buoyancy are positively correlated, i.e. small diaspores are less buoyant than large ones.

Table 3.  Correlations among diaspore traits for 12 mangrove species
 MassLengthRoot initiation (%)Shoot initiation (%)Buoyancy
  • *

    Spearman rank correlations.

Length−0.30    
Root initiation (%)+0.05−0.23   
Shoot initiation (%)+0.44−0.45+0.65  
Buoyancy*+0.69−0.05−0.20+0.14 
Time for root initiation*−0.09+0.23+0.87+0.63+0.14

Diaspore orientation and salinity

For Rhizophoraceae species with buoyant diaspores, orientation often changed from prone to vertical through time (Table 2, Fig. 2). These patterns were, however, variable among species during the course of the experiment but re-orientation was more marked in less saline solutions (Fig. 2). Three sinker species with elongated, but curved, diaspores never adopted a vertical position.

Figure 2.

Mean proportion of diaspores with vertical orientation in tanks of 100%, 50%, 10% and 0% seawater. Mean values shown from five diaspores placed in each of three replicate tanks.

Population effects on buoyancy

The effects of salinity treatments on buoyancy patterns were generally consistent across populations of a species (Table 4). Diaspores from both subtropical and tropical populations of R. stylosa and B. exaristata floated in full seawater, whereas A. marina sank and refloated and A. corniculatum sank in all treatments. Diaspores of R. stylosa showed interactions between population and salinity with higher proportions of diaspores sinking in more diluted seawater at subtropical latitudes. Despite some differences in details the overall buoyancy classification of species was consistent among populations from locations that were widely separated.

Table 4.  Summary of the effects of salinity on buoyancy of mangrove propagules from widely separated populations
 SalinityPopulationInteractionBuoyancy pattern
  1. NS = not significant, P > 0.05.

Aegiceras corniculatum<0.01NSNSSinker
Avicennia marina<0.01NSNSSinks and refloats
Bruguiera exaristata<0.01<0.01NSFloater
Rhizophora stylosa<0.001<0.01<0.05Floater

Initiation of roots prior to stranding

There were significant effects of both species (F12,143 = 22.1, P < 0.001) and duration of immersion on initiation of roots. Salinity, however, had little effect except for A. annulata (F3,8 = 16.0, P < 0.001), which developed roots only in full seawater, and A. corniculatum (F3,8 = 3.3, P < 0.1), which had few roots in full seawater.

Diaspores showed a wide range of times taken to develop lateral roots (dormancy) during enforced immersion (Table 2). A. marina had the shortest dormancy period, with 20% of diaspores developing roots by day 5, and X. mekongensis, a non-viviparous species, also had a short dormant phase (10–15 days with 17% of diaspores developing roots by day 10). By day 15 both species had initiated 4–5 roots per diaspore (4 and 40 mm long, respectively) whereas the other species had only one or two roots. All viviparous species had begun to develop roots by day 15 (Table 2). Of the remaining species, C. iripa and H. littoralis did not develop roots at all until day 23, and L. racemosa never showed signs of root or shoot development. Dissection of L. racemosa fruits revealed a viable embryo in 60% of fruits and this is therefore regarded as the only innately dormant species.

Apical development and early growth

There were significant effects of both species (F12,26 = 9.0, P < 0.001) and salinity on initiation of shoots following stranding (Fig. 3). The effect of salinity on the proportion of diaspores initiating apical shoots was significant at P < 0.05 for four species and for a further three species if probability of type one error was reduced to P < 0.1 (Table 5). The remaining species did not differ significantly in their response to the salinity treatments even if the high variances associated with some treatments are taken into account (P > 0.5). Trends in shoot emergence related to salinity are also shown in the shifting rank order of species in the proportion initiating apical shoots (Fig. 3). Most species initiate shoots at low salinity, but as salinity increases the number of species with greater than 25% of diaspores sprouting is reduced.

Figure 3.

Mean (SE) proportion of diaspores that initiated shoots after 15 days of enforced dispersal in tanks of (a) 100%, (b) 50%, (c) 10% and (d) 0% seawater. Species sorted in rank order of response.

Table 5.  Summary of the salinity effects on shoot initiation and growth 4 months after mangrove diaspore stranding
Species% Apical shoot initiation (SE)Apical shoot initiation in relation to salinityShoot growth index§ (mm/g fw)Initial shoot growth in relation to salinity
  • Ceriops australis was collected from dispersed propagules and this may confound comparisons. SE = standard error.

  • ‡Mean values averaged over all salinity treatments.

  • §

    §Index calculated as height of main shoot (mm) divided by mass of propagule (g fw).

  • *

    Significant difference P < 0.1,

  • **

    significant difference P < 0.05.

Aegialitis annulata15.0 (7.0)Few in fresh**11No growth in freshwater
Aegiceras corniculatum28.3 (9.9)Decrease with seawater*16Optimal growth 5% sw
Avicennia marina var. eucalyptifolia90.0 (5.2)No salinity effect20No salinity effect
Bruguiera exaristata75.0 (7.4)No salinity effect 6Optimal growth 5% sw
Bruguiera gymnorrhiza50.0 (11.1)Decease with seawater* 4Optimal growth 0–50% sw
Bruguiera parviflora28.3 (8.3)Optimal at 50% seawater** 2Optimal growth 0–50% sw
Ceriops australis63.3 (6.4)Decrease at 5% seawater* 1No salinity effect
Ceriops decandra36.6 (10.4)No salinity effect 2Optimal growth 0–50% sw
Ceriops tagal20.0 (6.0)No salinity effect 1Optimal growth 0–50% sw
Cynometra iripa21.7 (9.7)Decrease with salinity**12Optimal growth 0–10% sw
Heritiera littoralis15.0 (6.1)Decrease with salinity** 4Optimal growth 0–10% sw
Lumnitzera racemosaNoneNo initiation 0No growth
Rhizophora stylosa73.3 (7.9)No salinity effect 2Optimal growth 50–100% sw
Xylocarpus mekongensis81.7 (9.9)No salinity effect16Optimal growth 0–50% sw

Differences in growth (height of shoots) were observed among both species and salinity treatments (Fig. 4) but were not statistically tested because of the varied number of diaspores initiating shoots. Comparisons of the rank order of shoot height in relation to salinity show that some species have distinct tolerances for particular treatments (Fig. 4). Shoot height and diaspore weight are positively correlated and comparison of growth might therefore benefit from expressing height relative to diaspore weight, as in Fig. 5. This index of early growth takes into account the maternal storage effect of the diaspore, which may influence early seedling performance. Two species (A. annulata and R. stylosa) decreased while three species (H. littoralis, A. corniculatum and C. iripa) increased in their rank position from seawater to freshwater.

Figure 4.

Mean (SE) height of shoots in (a) 100%, (b) 50%, (c) 10% and (d) 0% seawater after 15 days of enforced dispersal and 15 weeks in early growth trays. Species sorted into rank order.

Figure 5.

Mean shoot height : fresh weight of diaspore ratios at (a) 100%, (b) 50%, (c) 10% and (d) 0% seawater after 15 days of floating and 15 weeks in early growth trays. Species sorted into rank order.

Relationship of diaspore traits and distribution

Correlations of abundance and habitat preferences within estuaries (Table 6) and individual diaspore attributes often showed contrasting signs but were rarely significantly correlated. Those species more abundant in the downstream end of estuaries were positively correlated with species that could initiate shoots over a range of salinities and could grow well in salinities greater than 10% seawater (Table 7). Conversely, those species abundant in the upstream locations of estuaries were positively associated with diaspores that grew taller in fresh and brackish water. Species more common in downstream locations were also less buoyant and were faster to initiate shoots than species more abundant in upstream locations.

Table 6.  Distribution and occurrence of mangrove species within and between estuaries in northern Australia. Bunt (1996) data are based on frequencies in 149 transects across 17 tidal waterways (estuaries) in north-east Australia. Wells (1995) data are from the presence in 82 tidal estuaries in northern Australia
 Position in estuary
(no. of sites)
Position in intertidal§
SpeciesCoastal range* (km)Frequency (fq among estuaries)Frequency (fq among sites)UpLowMidHighDownMid
  1. *Data from Tomlinson (1986), Wells (1995) and personal observations. †Data from Wells (1995). ‡Data from Bunt (1996). §Data from Duke 1995. −= absent from this region.

Aegialitis annulata 66000.970.148214 4 ++
Aegiceras corniculatum 74000.900.20273241+  
Avicennia marina100001.000.33533117+++
Bruguiera exaristata 48000.860.167327 0  +
Bruguiera gymnorrhiza 47000.390.45253936 ++
Bruguiera parviflora 41000.600.24354619 + 
Ceriops decandra 31000.470.22305713 ++
Cynometra iripa 13000.16 34354  +
Heritiera littoralis 22000.26 4 492  +
Lumnitzera racemosa 50000.800.09264826 ++
Rhizophora stylosa 70001.000.217026 4++ 
Xylocarpus mekongensis 48000.840.19195625 ++
Table 7.  Correlations of mangrove diaspore attributes and adult occurrences within estuaries, occurrences among estuaries and the range of species along the Australian coastline
 Frequency in sections of estuariesFrequency within estuariesFrequency among estuariesFrequency among estuariesCoastal range
 DownstreamMid-streamUpstream
  • *

    Significant correlation P < 0.05.

  • †Average values used across all salinity treatments.

Buoyancy−0.46+0.01+0.17+0.02+0.23+0.23−0.48
Time to initiate roots+0.55+0.07−0.42+0.39+0.23+0.17+0.43
Diaspore mass−0.09−0.14+0.17+0.31+0.40−0.01−0.59
Percentage root initiation+0.08+0.39−0.33+0.50+0.33−0.13+0.57
Percentage shoot initiation in freshwater−0.02+0.22−0.17+0.29+0.33−0.04−0.03
Percentage shoot initiation in 10% seawater+0.47+0.02−0.45+0.71*+0.67*−0.07+0.14
Percentage shoot initiation in 50% seawater+0.42+0.20−0.55+0.11+0.48+0.20−0.19
Percentage shoot initiation in seawater+0.59*−0.14−0.51+0.01+0.59*+0.65*+0.01
Shoot height in freshwater−0.53−0.12+0.59+0.05+0.14+0.13+0.11
Shoot height in 10% seawater−0.48−0.44+0.71+0.09+0.19+0.16+0.03
Shoot height in 50% seawater+0.30−0.01−0.28−0.01+0.42+0.15−0.01
Shoot height in seawater+0.31−0.08−0.25+0.03+0.54+0.34+0.24

Correlation of individual diaspore attributes and measures of relative occurrence of species within 17 estuaries (Bunt 1996) show a positive correlation with the ability to initiate roots and, in particular, shoot initiation in brackish (10% seawater) conditions. In contrast, the relative frequency of species occurrence among estuaries in the survey of Bunt (1996) was also positively correlated with shoot initiation and shoot growth in brackish (10% seawater) conditions (Table 7). In the more seasonally dry region, the relative frequency of species occurrence among estuaries (Wells 1995; n = 82 estuaries) was more strongly positively correlated with shoot initiation in full seawater (Table 7).

No strong correlations were detected between geographical range of species and early life history traits (Table 7).

Discussion

Are diaspore characteristics correlated?

Mangrove diaspores vary in weight and shape, and their ability to float and to initiate roots and shoots (Tables 1, 2 and 4). The expectation from terrestrial studies that larger diaspore weight would confer an advantage in root and shoot initiation (Westoby et al. 1997) was not consistently observed here, either within a phylogenetic group (six Rhizophoraceae species) or across different families (Table 3). Larger diaspores may, however, confer advantages in established life stages, such as resistance to predation, taller plants and larger leaf areas (Westoby et al. 1997). This covariation in traits needs to be measured in studies of other life history stages in tropical mangroves.

Do viviparous and non-viviparous diaspores have the same dispersal and early growth traits?

Many mangrove species have embryos that develop continuously without innate dormancy so that the dispersal unit is a seedling, or propagule, rather than a seed (Tomlinson 1986). However, not all mangrove species are viviparous and their dispersal unit, which is either a seed or a one-seeded fruit (Tomlinson 1986), may have some dormancy. Our study shows that, with the exception of the one dormant species (Lumnitzera racemosa), non-viviparous mangrove species show similar early growth traits to those of viviparous species. Ranges for buoyancy, seed weight, rates of root and shoot initiation, early growth and salinity tolerance also do not differ between the two classes. This finding is not consistent with the hypothesis of Joshi (1933) that selection for vivipary arises from escape from germination in saline habitats (see also Tomlinson 1986; Elmqvist & Cox 1996).

The presence of large viviparous diaspores in all Rhizophoraceae is related to their common descent, but similar traits are present in other lineages. This convergence may be related to the intrinsic instability of the regeneration niche selecting against small, dormant diaspores. The lack of dormancy in mangroves also appears to be consistent with the results of Rees (1994, 1997) who found that reduction in seed dormancy was associated with increased seed weight, efficient spatial seed dispersal and long-lived species.

Thirteen of the 14 mangroves tested had non-dormant diaspores, suggesting that these tropical forests have little or no buried seed bank and rely on regular cohorts of diaspores for regeneration. The absence of a seed bank in most mangrove stands reduces the temporal storage effect and increases the importance of early life history stages in determining spatial patterning within and among mangrove forest stands (for example Rabinowitz 1978a; Smith 1987; McKee 1995; McGuinness 1997; Clarke & Kerrigan 2000).

Are diaspore traits related to shoreline zonation?

We wished to assess whether shoreline zonation reflects differences in dispersal potential and subsequent stranding (Rabinowitz 1978a,b). In a review of mangrove structuring processes, Smith (1992) rejects dispersal effects and suggests that tidal action ‘delivers all species to all portions of the intertidal zone’. However, the 14 Indo-Pacific species tested showed a range of buoyancy patterns, from floating for prolonged periods to sinking, and the combined effects of buoyancy, diaspore weight and differences in the time taken to initiate shoots and roots, could influence stranding patterns across the shoreline. These patterns could, in turn, reflect intertidal habitat differentiation (zonation) by dispersal sorting in the absence of physiological tolerance, predation and competition.

Discussion of tidal sorting and zonation assumes that shoreline zonation occurs. In a recent analysis, Bunt (1996) showed that species sequences across an intertidal location are highly variable and that multiple centres of distribution often occur. It is now clear that shore parallel species sequences (zonation sensu stricto) are not as consistent as portrayed in general accounts of mangrove shore zonation (see Watson 1928; Chapman 1976 for patterns and Macnae 1966; Semeniuk 1985; Bunt et al. 1991; Ellison et al. 2000 for exceptions). Nevertheless, several of the species used in the present study (C. iripa, L. racemosa, H. littoralis) consistently occur high on the shore, whilst others (R. stylosa, A. marina) commonly extend from low to high shore locations (Duke 1992; Bunt 1996) (see Table 6).

The diaspore dispersal potential characteristics of weight, shape, orientation and buoyancy appear unrelated to shore parallel species zonation in northern Australia. For example, species with small diaspores (for example A. corniculatum, A. annulata and L. racemosa) are not restricted to high shore habitats as suggested by Rabinowitz (1978a) and are generally less buoyant than species with large diaspores. Similarly, species with diaspores that float (for example R. stylosa, A. marina and B. gymnorrhiza) are not restricted to high shore habitats. Whilst dispersal potential alone does not correspond with zonation, the combination of buoyancy and early growth may account for the distribution of some high shore species (C. iripa, H. littoralis, L. racemosa). These species all float for long periods and initiate roots and shoots more slowly than other floating species. Growing these species in intertidal locations will test whether they are restricted to the backshore because of physiological tolerance, predation, or competition from low shore species. In general, however, the effect of tidal sorting of diaspores on shore parallel zonation does not appear to be important for low and mid-tidal mangrove species in northern Australia.

Are diaspore traits related to river zonation?

Habitat differentiation of mangrove species along rivers has been shown to have some basis from the systematic surveys of rivers in northern Australia (Bunt 1996) and may be related to salinity tolerance (Bunt et al. 1982). The habitats for 12 of the species used in this study are shown in Table 6 (Bunt 1996) and several have upstream distributions (A. corniculatum, C. iripa, H. littoralis) whilst others are more frequent downstream (A. annulata, A. marina, B. exaristata and R. stylosa). Upstream locations are more likely to experience more freshwater influence, although caution should used because seasonal aridity can ‘reverse’ salinity gradients in some monsoon estuaries (Duke 1992).

Dispersal potential traits (diaspore buoyancy and timing of root initiation) showed little relationship with the relative frequency of species in down stream, mid-stream and upstream locations (Table 7). The tendency of some species (B. exaristata and C. decandras) to have diaspores that sink in freshwater does not correspond with the distribution of these species along the estuary gradient (Table 6).

The differential growth responses to salinity observed in many species generally correspond to results in culture (see review by Smith 1992). Salinity preferences at the early growth stages can, however, only be directly related to river zonation in a few cases. For example, A. annulata was rarely found upstream and will not grow in freshwater, whereas C. iripa and H. littoralis are commonly recorded in upstream locations and grew best at low salinities. Across all species there was a positive correlation between species abundances in the downstream sections of estuaries and the initiation of shoots in full seawater (Table 7). Conversely, upstream abundance was negatively correlated with initiation and growth shoots in seawater.

Growth in relation to salinity has been used to explain the river zonation of Sonneratia (Ball 1995) and Ceriops congeners (Smith 1988) and unrelated sympatric species (Hutchings & Saenger 1987; Ball 1988; Ball et al. 1988). Alone, however, tolerance of edaphic conditions is unlikely to explain distribution because dispersal properties, early growth abilities and susceptibility to predators vary among species. It is clear, however, that salinity during dispersal and stranding affects early growth of mangrove species in different ways. Recently, the combined effects of dispersal potential and early growth of diaspores have been used to explain the distribution of co-occurring mangroves (Clarke 1995; McKee 1995) and smaller scale patterning (Minchinton 2001). Thus, field experiments on the effects of dispersal properties, early growth abilities, tolerance of edaphic conditions and predation are needed to clarify river, as well as shore, zonation.

Do diaspore traits influence distribution and abundance at larger spatial scales?

The occurrence of mangrove species in northern Australia is often sporadic among estuaries within their geographical range (Wells 1995; Bunt 1996). Some species occur commonly within their geographical range but are less frequent within estuaries (for example, R. stylosa), whilst others have more sporadic occurrences across their geographical range but are more frequent within those estuaries where they occur (for example, B. gymnorrhiza) (Table 6). Wells (1995) suggests that although species with restricted discontinuous distributions could disperse to all estuaries, seasonal salinity leads to patchy distribution. Our study also suggests that dispersal potential was not related to species occurrences within or between estuaries but may be related to early growth.

Species with the ability to initiate shoots and grow in seawater appear to be more abundant in the monsoonal estuaries sampled by Wells (1995). This pattern is also significant in the less seasonal estuaries of Bunt’s study, where the ability to initiate roots and shoots under low salinity conditions is also related to frequency of occurrence. These results suggest that some species are unable to colonize from supply populations because of the inhibitory effects of full seawater on early growth. This may account for the under-saturation of species in estuaries with suitable habitats. This hypothesis is counter-intuitive to the way distant dispersal often occurs, as those seeds that are dormant have more time to be widely dispersed. In unstable habitats, such as mangroves, lack of dormancy in the dispersal medium (seawater) may be advantageous, as it would increase the chance of successful early growth upon stranding in a favourable site.

Finally, the geographical range of our study species varied from a few thousand kilometres to about 10 000 kilometres along the continuous Australian coastline. This range of distribution was, surprisingly, negatively correlated with buoyancy and diaspore weight. This negative correlation suggests that geographical limits to the early growth of mangrove species are independent of their dispersal abilities. Across all spatial scales early life history traits of 12 mangroves showed poor correlation with patterns of adult distribution. Traits related to establishment tended to be stronger predictors of occurrence than those associated with dispersal.

Acknowledgements

We wish to thank the staff at the Australian Institute of Marine Science (AIMS) for their support throughout the project. In particular we are grateful to Barry Clough, Dan Alongi, Janet Ley and Alistair Robertson, for sponsorship at AIMS and logistical support. We are indebted to Paul Dixon and to Otto Dalhaus for diaspore collection and their contribution to the care of mangrove seedlings. Graeme Wells and John Bunt had the vision to collect mangrove distribution and abundance data in remote regions of the Australia. The Queensland Department of Primary Industries and the National and Marine Parks Services granted permission for diaspore collection. The project was funded by an Australian Research Council grant A19530936.

Received 26 June 2000 revision accepted 7 February 2001

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