Austral Ecology

(2003)

28

, 271–280

Seed production and germination in two rare and three common co-occurring

Acacia

species from south-east Australia

J. BROWN, N. J. ENRIGHT* AND B. P. MILLER

School of Anthropology, Geography & Environmental Studies, University of Melbourne, Parkville 3010, Australia (Email: neal@unimelb.edu.au)

Abstract

Seed set, size, viability and germination requirements were investigated for two rare (

Acacia ausfeldii

and

A. williamsonii

) and three common (

A. pycnantha

,

A. genistifolia

and

A. paradoxa

) co-occurring congeners in box–ironbark eucalypt forests near Bendigo, south-east Australia to investigate correlates of rarity. Seed size wassignificantly smaller for the two rare species and germinants were less able to emerge from deeper sowing depthsthan were the larger seeded common congeners. All species had a strong heat-stimulated germination response. Whilethe rare

A. ausfeldii

showed strong germination only at the highest temperature treatment (100

�

C), the

common

andwidespread

A. pycnantha

showed strong germination across a

broad

range

of

temperatures (60–100

�

C), likely

to

beexperienced

by

soil-stored

seeds

during

a

fire.

Seed

viability,

number

of seeds per plant, and number of firm,aborted and eaten seeds per pod varied between species, but the pattern of variation was not related to rarity. Smallseed size and a very specific temperature requirement for germination may help to explain rarity in

A. ausfeldii

, andto a lesser extent in

A. williamsonii

. Fires are often patchy and heating of the soil is likely to be highly spatially variable,so species with germination responses to a broad range of temperatures have an advantage over those that respondonly to a narrow range. A narrower range of soil depths from which seeds can emerge will further reduce theproportion of the seed bank that might recruit following fire. Human impacts on species habitats, such asfragmentation, loss of topsoil through mining, timber harvesting, grazing and urbanization, and consequentreduction in fire intensity, are likely to have further contributed to rarity in these species. The role of pollination andother factors in relation to population size is the subject of further investigation.

Key words:

Acacia

, fire, forms of rarity, heat stimulated germination, seed set, seed size.

INTRODUCTION

The explanation of why some species are rare whileothers are common is central to the conservationmanagement

of

plant

species

and

is

fundamental

toour understanding of the dynamics of species andcommunities. Rabinowitz (1981) described sevenforms of rarity, documenting patterns of geographicalextent, local abundance and habitat specificity as keyattributes in identifying different types of rarity.However, except for habitat specificity, these categoriz-ations of rarity do not provide any explanation of whysome species are less abundant, and/or less widelydistributed than other, often closely related, species.Many biological and ecological traits of rare plantspecies have now been implicated in such explanations(Gaston 1994; Kunin & Gaston 1997; Bevill & Louda1999; Murray

et al

. 2002). Among these are: habitatloss; fragmentation and small habitat area effects,including

impacts

of

pollinator

availability

(Milberg

&

Bertilsson 1997; Cunningham 2000a) and pollenquantity (Brown & Kephart 1999) on seed-set andviability; poor competitive ability (Rabinowitz & Rapp1981; Prober & Austin 1993; Lynch

et al

. 1999);habitat conditions affecting establishment, such astolerance to shading and dense litter (Dinsdale

et al

.2000); dependence on specific seed dormancybreaking mechanisms (e.g. fire) to trigger germination(Cropper 1993; Lynch

et al

. 1999); and increasedfrequency

of

disturbance

leading

to

plant

deathbefore reproductive maturity (Enright

et al

. 1996).Small or reduced populations may be further threat-ened because of the genetic consequences of self-incompatibility,

genetic

drift

and

accumulation

oflethal genes (Les

et al

. 1991; Ellstrand & Elam 1993;Oostermeijer

et al

. 1998; Giblin & Hamilton 1999;Kery

et al

. 2000). Recent speciation and the absence oftime for spread (neo-endemism) may also explainrarity (e.g. Kruckeberg & Rabinowitz 1985; Prober

et al

. 1990; Witkowski & Lamont 1997), in which casethis list of biological traits would not necessarily berelevant. Further, common species may show some orall of the traits expected of rare congeners (e.g. low

*Corresponding author.Accepted for publication November 2002.

272 J . BROWN

ET AL.

seed production, low pollinator visitation, smallflowers, low pollen/ovule ratios in common

Rhodo-dendron

species from Hong Kong; Ng & Corlett 2000)and

vice versa

(e.g. high genetic diversity in the rare

Acacia anomala

in south-west Australia; Coates 1988),so that broad generalizations are perhaps as yet unwar-ranted, and more comparative studies are needed inorder to distinguish between causal correlated anduncorrelated attributes (Bevill & Louda 1999).

Three approaches to determining causes of rarity aredemonstrated in the literature: (i) an examination of theattributes of a single rare species and an interpretationthat rests on traits that the author feels may be theweakest link in the life-cycle; (ii) a comparison of arange of specific traits across several species, usuallyeither congeners or otherwise phylogenetically inde-pendent contrasts; and (iii) a large-scale comparisonacross an entire flora that relates general traits to thearea of distribution of each species.

Large-scale, phylogenetically (or taxonomically)corrected

comparative

studies

of

traits

correlatedwith rarity have been conducted for three European(Kelly & Woodward 1996; Jakobsson

et al

. 1998) andone South African (Cowling & Eggenberg 2000) flora.The assumption that limited distribution equals rarityclouds the first of these analyses, whereas, in the secondthe major correlates are mostly descriptors rather thanbiological traits associated with rarity (e.g. low abun-dance in the habitat). The final analysis is restricted toa single trait (seed : ovule ratio) but claims that contra-dictory generalizations about rarity can be resolved byanalysing comparisons separately for different forms ofrarity. Comparative studies focusing on either a smallnumber of species within a single genus (Lee & Cavers1981;

Fiedler

1987;

Byers

&

Meagher

1997;

Young& Brown 1998; Ng & Corlett 2000; Osunkoya &Swanborough 2001), or paired species across genera(Baskin

et al

. 1997) do not produce a consensus oncauses of rarity. Nevertheless, reproductive traits,which are the focus of most such studies, have providedthe best evidence of factors that correlate with rarity.

Studies addressing rarity generally focus on the morereadily quantifiable reproductive characters. Other life-history attributes such as mean longevity, time to firstreproduction, length of reproductive period, juvenileand seedling survivorship, and adult mortality are lessfrequently analysed. This bias persists despite analysesof relative contribution to population growth rates forlonger lived plant species showing that survivorship-and growth-related traits invariably surpass fecunditytraits in importance (Silvertown

et al

. 1993, 1996).Using a comprehensive life-cycle analysis Byers andMeagher (1997) determined that although survivaltraits were most important in the short-term survival ofa rare perennial plant, seed production and coloniz-ation of new sites would be important in the long term.

It is clear that further comparative case studies are

required across the range of Rabinowitz’s (1981) sevenforms of rarity, and covering a more complete range oflife history traits, before correlates and causes of raritymay be more securely generalized.

As indicated, the majority of studies identify thereproductive (pollination biology, seed production,dispersal and survival) and recruitment (germinationand establishment) phases of the plant species’ lifehistory as the most likely to explain rarity. The presentpaper focuses on seed attributes (seed production,viability and germination) in two rare and up to threecommon coexisting congeners as correlates of rarity.

Acacia ausfeldii

Regel and

A. williamsonii

Court arerestricted endemic shrubs of box–ironbark (

Eucalyptusmicrocarpa – E. tricarpa

) open forests in centralVictoria, south-eastern Australia. Their ranges(approximately 190 km east–west

�

100 km north–south for

A. ausfeldii

and approximately 170 km east–west

�

45 km north–south for

A. williamsonii

) arerelatively small, as is the number of known extantpopulations (39 and 31, respectively). Only nine

A. ausfeldii

and

A. williamsonii

populations exceed1000 individuals (Briggs & Leigh 1995).

Acaciaausfeldii

and

A. williamsonii

are understorey shrub-layercomponents of heavily disturbed forest sites associatedwith a 150-year history of human impacts from goldprospecting and mining, timber harvesting, sheep andcattle grazing, and land clearance. Populations of thesespecies

are

generally small (50–2000 individuals),and are fragmented. The factors that limit the geo-graphical extent and abundance of these species withinthe poor sedimentary soils and relatively low rainfall(450–550 mm) of the box–ironbark ecosystem (whichextends considerably east and west of the speciesranges) are not known. Although many of the popu-lations are small, according to Rabinowitz’s sevenforms of rarity (Rabinowitz 1981), rarity in thesespecies is more due to restricted range and habitatrather than small population sizes.

Several widespread and common congeners,including A. pycnantha Benth, A. genistifolia Link andA. paradoxa DC., frequently co-occur with theserestricted species. All of these species are killed by fireand depend upon seeds for recruitment (Bell et al.1993). They are hard-seeded and seeds accumulate ina dormant soil seed bank. Heat from fire ruptures theseed coat, allowing imbibition of soil water and germin-ation, typically during the first winter–spring after fire(Auld & O’Connell 1991). Thus stands develop assingle-aged cohorts with plant age the same as timesince last fire. Some interfire germination of seeds mayoccur in long-unburned stands because of age-relatedscarification of seeds stored in the soil, so that multi-aged stands might develop in the prolonged absence offire. Failure of interfire recruitment in long unburnedstands would result in local extinction as the postfirecohort senesces.

SEED PRODUCTION AND GERMINATION IN ACACIA 273

In the present study we investigate the followinghypotheses:1. That rare species produce fewer seeds per plantthan common congeners and show higher variation inlevels of seed set within populations (e.g. Kery et al.2000).2. That rare species have higher levels of seedabortion and lower seed viability than common species(e.g. Oostermeijer et al. 1998).3. That levels of on-plant seed predation (granivory)are higher in rare species than in common congeners.Cunningham (2000a) reported lower granivory forsmall, fragmented populations of Acacia brachybotryain eastern Australia, and seed predators might beexpected to have evolved more readily in associationwith common species. However, rare species may behighly susceptible to impacts from generalist granivoreswhere related rare and common species co-occur.4. That rare species are characterized by smaller seedsize than common congeners (Rabinowitz & Rapp1981). Large seed size should confer an advantage inrecruitment and survival through greater provisioningof the seedling.5. That if rare species are characterized by smallerseeds, then these seeds are also more limited interms of the soil depths from which they canemerge relative to larger seeded congeners (Musil &De Witt 1990; Bond et al. 1999). Shallow emergencecapability may limit the size of the regenerationniche by restricting successful recruits to a narrowerrange of soil burial depths (proportionately, moreseeds will be located either too deep to recruit even ifsoil heating triggers germination, or in near-surfacelocations that may receive lethal temperatures duringfires).6. That rare species have more specific heat require-ments for breaking of dormancy, that is, a narrowerregeneration niche. Variations in fire intensity and even-ness of soil heating (Tozer 1998) may restrict thespatial distribution of germination so that the speciescan occupy only a small part of the landscape, or bepresent at low density.

METHODS AND STUDY AREA

Study species and area

Acacia ausfeldii is listed as vulnerable in Victoria andrare in Australia, whereas A. williamsonii is regarded asrare at both State and National levels according to thelist of Rare or Threatened Australian Plants (ROTAP;Briggs & Leigh 1995). In south-east Australia bothspecies occur as fragmented populations (30–40known localities) of small geographical extent, butsometimes of high abundance (23% of A. ausfeldii

populations and 45% of A. williamsonii populationscontain >1000 individuals), in the heavily disturbedbox–ironbark forests of central Victoria in and near thecity of Bendigo (S. Berwick, pers. comm., 2000).Acacia genistifolia, A. pycnantha and A. paradoxa arecommon, widespread and abundant in Victoria. Allfive species flower in late winter to early spring(August–September) and seeds are dispersed in earlysummer (November–December). Acacia williamsoniishares morphological affinities with A. pycnantha,whereas A. ausfeldii shares morphological affinities withA. genistifolia and A. paradoxa (Costermans 1998).Although phylogenetic relationships within the groupare not fully known, both rare species are thoughtto be closely related to more broadly distributed andcommon species (Costermans 1998). Four of thespecies are understorey shrubs to approximately 3 mheight. The fifth, A. pycnantha, is an understorey treeto 8 m and is characterized by larger phyllodes thanoccur in the other species.

Methods

Field

Plant height, mean canopy diameter (averaged over twomeasurements at right angles to each other), andnumber of seed pods were enumerated for 50–100individuals of these co-occurring Acacia species withinsites at Salomon Gully Reserve (36�46�S, 144�16�E)and Whipstick State Park (36�39�S, 144�16�E), nearBendigo in south-east Australia. Sampling started froma random individual, with nearest-new-neighboursampled in turn until no further individuals couldreadily be located nearby. Species sampled atSalomon Gully Reserve were A. ausfeldii, A. genistifolia,A. paradoxa and A. pycnantha, and at Whipstick StatePark were A. genistifolia, A. paradoxa, A. pycnantha andA. williamsonii (i.e. the common species were allpresent at both sites). Samples of approximately 25closed seed-pods were collected from each of four partsof the plant canopy for each of 10 plants for eachspecies at both sites.

Laboratory

Seed pods collected from individuals in stands atSalomon Gully and Whipstick State Park were allowedto dry for 48 h at room temperature, and a randomsample of 10 pods per plant was then opened and theseeds counted into three categories: firm (plump seedscontaining endosperm), aborted (brittle and light withno endosperm apparent), and eaten (frass indicatingconsumption of a firm seed by insect larvae). Firmseeds were extracted from the remaining pods andbulked for viability testing.

274 J. BROWN ET AL.

Seed viability was estimated for five batches of 20seeds from each species. Seed coats were nicked with ascalpel (scarified) to expose the endosperm. Seedswere placed in Petri dishes on Whatman no. 1 Qualita-tive filter paper kept moist with a mix of de-ionizedwater and a 1.5-g l–1 solution of Mancozeb fungicide,and germination tested under a 24-h dark regime in anincubator at 20�C. Germination was recorded every2 days for 2 weeks, or until no new germinants werenoted over two successive 2-day periods once germin-ation had commenced.

Samples of seeds collected from three localities(populations) in 1999–2000 for four of the five species(excluding A. paradoxa) were used to test the role ofheat in germination. Seed germination in Acacia speciesis normally cued to fire: the heating of soil-stored seedsbreaking the dormancy enforced by the hard seed coat.Samples of 100 seeds from each population and specieswere heated at 60, 80 or 100�C for 5 min in aluminiumtrays in a drying oven. This duration and temperaturerange combination was found by Auld and O’Connell(1991) to produce the optimum germination responsesfor a broad range of hard-seeded Australian nativeplant species. Seeds were divided into five batches of20 seeds per population per species, and germinationwas traced weekly for 8 weeks following the sameprocedure as described above for viability.

A control sample of 100 seeds from each populationand species was also established, which was stored at20�C and given no heat treatment. Because heat treat-ments were administered to batches of 100 seeds, theirsubsequent division into five replicates of 20 seeds doesnot meet the requirements of true sample replication

(Morrison & Morris 2000) and constitutes pseudo-replication only. True replication would require thateach batch of 20 seeds be heated on separate occasions,or in different ovens. Therefore, we combined the datawithin populations for the purposes of analysis, so thatreplication for each species and treatment is describedby the three populations of 100 seeds per treatment.

Freshly germinated seeds from each species (for asingle population source per species) were sown in fourbatches of 10 germinants per sowing depth in soil-filled(Hortico potting mix) pots at depths of 2, 4 and 8 cm,respectively, to determine the burial depths from whichgerminating seeds might successfully emerge. Potswere placed in a glasshouse and watered twice daily byan automatic sprinkler system. Pot locations wererandomized and emergence was traced for 8 weeks.The method followed was similar to that described byAuld (1986).

Nested Analysis of Variance (ANOVA), with Tukeycorrected post hoc comparison of means, and two-wayANOVA (SYSTAT 10; SPSS 2000), were used to comparethe various seed-related parameters for each species.Assumptions of normality were investigated withstandard techniques, and transformations used asnecessary.

RESULTS

Because sample data were collected from mature standswhere up to four of the Acacia species co-occurred, weassumed that individuals from each species were ofsimilar maximum age, and that this age reflected time

Table 1. Percentage of individuals from five Acacia species setting seed in 2000 in relation to plant height, for two mature standsnear Bendigo, south-east Australia

Species n Height class 1 Height class 2 Height class 3

A. ausfeldii 50 18 92 100A. genistifolia 105 20 65 91A. paradoxa 50 33 84 93A. pycnantha 105 0 33 44A. williamsonii 70 20 60 67

Height classes are scaled (1 = small to 3 = large) according to maximum height for each species as descr ibed in the text.

Table 2. Minimum size (height) of reproductive individuals, and number of seed pods (± SE) produced per individual ofreproductive size, for five Acacia species from two mature stands near Bendigo, south-east Australia

Species n Minimum reproductive size (m) Seed pods per plant CV

A. ausfeldii 44 0.40 57.4 ± 59.5a 1.04A. genistifolia 89 0.35 27.2 ± 38.4b 1.42A. paradoxa 47 0.15 21.0 ± 21.2b 1.01A. pycnantha 66 1.20 11.7 ± 25.8b 2.20A. williamsonii 69 0.60 25.7 ± 80.9b 3.15

Column values followed by the same letter are not significantly different (one-way ANOVA with Bonferroni-corrected post hoccomparison of means; P < 0.05).

SEED PRODUCTION AND GERMINATION IN ACACIA 275

since last fire (most individuals recruit in the firstwinter following fire). Thus, plants had had the samemaximum time for growth and had all grown under thesame set of environmental conditions. Because eachspecies is somewhat different in habit, a direct com-parison of the relationship between plant size andfecundity is not possible. Here, individuals from eachspecies were allocated to one of three height classes,scaled by maximum height for the species in thesampled areas, within which a percentage of individualsare compared (Table 1). Acacia pycnantha (maximumheight 4 m) and A. williamsonii (3.2 m) were the tallestspecies, A. ausfeldii (2.4 m) was intermediate andA. genistifolia (1.65 m) and A. paradoxa (1.55 m) werethe smallest. Height classes used were 0–1, 1–2 and >2m for the tallest species, 0–0.75, 0.75–1.5 and >1.5 mfor A. ausfeldii, and 0–0.5, 0.5–1 and >1 m for thesmallest species. In all species, the probability ofsetting seed increased with plant size. However, whilealmost 100% of large individuals from the threesmallest species set seed, only 44 and 67% of largeindividuals from the tallest species set seed, respec-tively. The two rare species showed strongly contrastingbehaviour; nearly 100% of A. ausfeldii individuals in thesecond and third height classes set seed, while only60 and 67% did so in A. williamsonii. The lowest seedset was in the common and widespread speciesA. pycnantha.

The minimum height of reproducing individualsparalleled the distribution of maximum heights amongthe five species, being least in A. paradoxa (0.15 m) andgreatest in A. pycnantha (1.20 m; Table 2). Mean(± SE) number of seed pods set by individuals ofreproductive size was highest for the rare A. ausfeldii(57.4 ± 59.5) and lowest for the common A. pycnantha(11.7 ± 25.8). The coefficient of variation for numberof seed pods per plant was highest for the other

rare species, A. williamsonii (3.15), and lowest forA. paradoxa (1.01) and A. ausfeldii (1.04; Table 2).

The mean number of potential seeds (firm seeds +eaten + aborted) per pod varied among the fivespecies tested from 5.23 ± 0.16 for Acacia paradoxa to9.00 ± 0.22 for A. pycnantha (Fig. 1). The two rarespecies, A. ausfeldii and A. williamsonii, had inter-mediate numbers of seeds per pod, as did thecommon A. genistifolia. Differences among speciesand differences among plants (within species) weresignificant in a nested ANOVA (F4,45,450 = 72.84, 6.18,P < 0.001). Tukey post hoc tests indicate that while thetwo rare species did not differ from one another, thecommon species all differed from each other, as well asfrom the rare species (all P < 0.001, except A. ausfeldiiand A. genistifolia where P = 0.018). Although therewere more seeds per pod for A. pycnantha than foreither rare species, testing species nested within rare/common indicated that rare species had higher seedproduction per pod (7.730 ± 0.14 seeds) than thecommon species (7.033 ± 0.11; ANOVA F1,3,495 = 14.86,61.10, P < 0.001).

The proportion of seeds in each pod that were firm,eaten and aborted were compared among species;however, as potential firm (firm + eaten) is equal to1 – proportion aborted, this was not tested separately.Nested ANOVA of the Arcsine transformed propor-tions indicated significant differences within andamong species in each case (nested ANOVA amongspecies F4,450 = 9.4,4.0,19.4, P < 0.001; firmP < 0.001, aborted P = 0.004, eaten P < 0.001,respectively; Table 3). The smallest differences werein aborted seeds (range 22–34%: and hence inpotential firm seeds) where A. ausfeldii and A. paradoxahad > 30% abortion, and A. genistifolia had 22%. Theproportion of seeds eaten was less than 10% (lowest inA. ausfeldii, 2%) in all species except for A. williamsoniiin which 15% of seeds were consumed in the pod.Reflecting these patterns, A. williamsonii, A. ausfeldiiand A. paradoxa had the lowest proportion of firmseeds within pods and A. genistifolia the highest (range56–75%).

The mean number of firm seeds differed significantlyamong species and plants within species (nested

Fig. 1. Mean total seeds per pod, and mean firm, abortedand eaten seeds per pod for five Acacia species from box-ironbark forests near Bendigo, south Australia (n = 100 podsper species). Error bars are ± SE. ( ), Total seeds; ( ), firm;( ), aborted; (�), eaten.

Table 3. Mean proportion (%) of firm, aborted and eatenseeds per pod for five Acacia species from two mature standsnear Bendigo, south-east Australia

% Firm % Aborted % Eaten

A. ausfeldii 63.4ab 34.4b 2.1ab

A. genistifolia 74.6c0 22.1a 3.3ab

A. paradoxa 58.9ab 32.6b 8.5b

A. pycnantha 66.7bc 28.3ab 5.2ab

A. williamsonii 56.4ab 28.2ab 15.4c

n = 100 for each species. Species that do not differ shareletter codes (Tukey post hoc test P < 0.05).

276 J. BROWN ET AL.

ANOVA F4,36,459 = 31.1,4.7; P < 0.001), varying twofoldfrom A. paradoxa (2.98 + 0.17) to A. pycnantha(6.06 ± 0.28). The only significant (Tukey P < 0.001)pairwise differences were between these two speciesand all others. The remaining three, including both rarespecies had 4.4–5.1 seeds per pod (Fig. 1).

Multiplying mean likelihood of setting seed (Table 1)by mean pod production (Table 2) and mean firmseeds (Fig. 1) gave an estimate of mean firm seedproduction per plant. In the largest height class thesewere highest for A. ausfeldii (approximately 275 seedsper plant), twice the production of the next highest,A. genistifolia (approximately 130), which wasfollowed by A. williamsonii (76), A. paradoxa (58) andA. pycnantha (31).

Mean seed weight (including elaiosome) was signifi-cantly different among the five Acacia species testedand rare species had significantly lower seed mass (lessthan half, on average) than common species (nestedANOVA; F1,3,45 = 90.8, 7.23; P < 0.001). The two rarespecies, A. ausfeldii and A. williamsonii, had thelowest seed weights (Fig. 2). Acacia genistifolia andA. pycnantha had the highest seed weights, while seedsof A. paradoxa were intermediate. Results were con-

sistent with those reported for four of these five speciesby Brown (2000).

Seed viability, estimated as germination rate for firm,scarified seeds, ranged from 69% for A. ausfeldii (rare)and A. genistifolia (common) to 99% for A. pycnantha(common). Although there were significant differencesin germination level among species, there was noconsistent difference in relation to rarity, withA. williamsonii (rare) showing high viability (96%) andA. genistifolia low viability (ANOVA: d.f. = 3,16,F3,16 = 45.9, P < 0.001). Control samples showedgermination rates of 0–3% and were significantlydifferent from scarified samples.

Proportions of germinants emerging from soil depthsof 2, 4 and 8 cm among the four species (A. ausfeldii,A. genistifolia, A. pycnantha and A. williamsonii) alldeclined significantly as burial depth increased (Fig. 3,Table 4). The pattern of decline in emergence withdepth did not differ significantly with rarity, and onlyslightly (P = 0.048) between species within rare andcommon. Emergence was lowest overall for the tworare species and was significantly different from

Fig. 2. Mean seed weight among five co-occurring rare andcommon Acacia species from two stands near Bendigo, south-east Australia. Error bars are SD, means that are not signifi-cantly different are indicated by the same letter above theerror bar (post hoc comparison of means, Bonferronicorrected).

Fig. 3. Mean number of germinants emerging from threesowing depths for four Acacia species from mature standsnear Bendigo, south-east Australia. Error bars are ± SE. ( ),2 cm; ( ), 4 cm; (�), 8 cm.

Table 4. Analysis of variance table for comparison of seedling emergence from 2, 4, and 8 cm burial depth among four Acaciaspecies (nested within rare vs common: two rare, two common) from mature stands near Bendigo, south-east Australia

Source d.f. Mean-Square F-ratio P

Rare/Common 1 114.083 69.610 0.000*Depth 2 157.562 96.140 0.000*Depth � Rare/Common 2 3.146 1.919 0.1610Species (Rare/Common) 2 37.667 22.983 0.000*Depth � Species (Rare/Common) 4 4.354 2.657 0.048*Error 36 1.639

*Significant differences.

SEED PRODUCTION AND GERMINATION IN ACACIA 277

emergence rates for the common species (P < 0.001:Table 4). There was no emergence for A. ausfeldii from8 cm and <10% emergence for A. williamsonii fromthis depth. In contrast values for the common specieswere 22 to 50%. Across all depths, emergence wasstrongest in A. pycnantha with close to 100% emer-gence from 2 and 4 cm and 50% emergence from 8 cmdepth.

Exposure of seeds to heat led to significantlyincreased levels of germination relative to untreatedcontrols, with highest levels of germination recordedfor the 100�C treatment in all four species tested(Fig. 4, Table 5). Controls showed a mean germinationresponse of 2.1–6.3% with significant differencesamong species. Acacia ausfeldii showed only a smallincrease over the control germination level at 60�C and80�C (both 6.3%), but a higher response (21.3%) at100�C. However, even at 100�C there was still highvariation in germination response among the threepopulations for this species, with one populationrecording a rate of 38% and the other two only 12–14%.Acacia pycnantha showed the highest response to heattreatments overall (up to 49% germination at 100�C),

with germination increasing markedly over controls forall treatments (Fig. 4). This difference in responseamong species to the 60�C and 80�C treatments inparticular was reflected in a significant interactioneffect between species and treatment (Table 5).

DISCUSSION

Results presented here support the contention that rarespecies are likely to have smaller seeds than commoncongeners (Rabinowitz & Rapp 1981). Acacia ausfeldiiand A. williamsonii had the lowest mean seed weightsand these were significantly different from the seedweights for the three more common species. Small seedsize means lower provisioning of the seedling withresources for early growth and so might represent adisadvantage in establishment and first year survival.Production of smaller seed is often associated withgreater seed production (Leishman 2001): thisobservation was borne out in the case of A. ausfeldii,but not A. williamsonii. Another potential outcome ofsmall seed size is that seeds are more limited in termsof the soil depths from which they can emerge relativeto larger seeded species (Musil & de Witt 1990; Bondet al. 1999). Results here support this contention also,with germinants from the two rare species usuallyfailing to grow to the soil surface if sown at a depth of8 cm, whereas larger seeded congeners all recruitedsome individuals that were sown at this depth. Lowseed capital reduces the size of the regeneration nicheby limiting successful recruits to a narrower range ofsoil burial depths.

It may be hypothesized that smaller seeds infiltratecracks in the rocky/clayey box–ironbark soils to greaterdepth than do larger seeds. However, given that Acaciaseed dispersal (and burial) is largely attributable to ants(Berg 1975), and given our limited knowledge of thetypical range of depth of burial of these species, we canonly assume no difference in the burial depths forco-occurring Acacia species with different seed sizes.With this assumption, and our seed emergence data, itappears that relative to large-seeded (common) species,proportionately more seeds of the small-seeded (rare)

Fig. 4. Mean number of germinants for samples of 100seeds in relation to heat treatments for four Acacia speciesfrom three mature stands near Bendigo, south-east Australia.(�), Control; ( ), 60�C; ( ), 80�C; ( ), 100�C heat treat-ments. Error bars are ± SE.

Table 5. Analysis of variance table for comparison of seed germination in relation to heat treatment (control, 60, 80, 100�C)among four Acacia species (nested within rare vs common: two rare, two common) from mature stands near Bendigo, south-eastAustralia

Source d.f. Mean-Square F-ratio P

Rare/Common 1 397.728 12.658 0.001*Heat 3 1537.928 48.945 0.000*Heat � Rare/Common 3 58.147 1.851 0.1580Species (Rare/Common) 2 1112.160 35.395 0.000*Heat � Species (Rare/Common) 6 113.649 3.617 0.007*Error 32 31.422

*Significant differences.

278 J. BROWN ET AL.

species would be too deep for them to recruit even ifsoil heating triggers germination. Tozer (1998)reported that approximately 80% of seeds of Acaciasaligna were located within 6 cm of the soil surface, andthat 88–94% of the seed bank remained dormantfollowing heating in a field experiment that sought tosimulate fire effects on recruitment in this species. Thisis likely to be a result of a combination of factors suchas depth of seed burial, germination requirements, seedviability and fire heterogeneity. The latter is influencedby fuel type, soil moisture and other on-site conditions,and will vary within and between sites (Auld &O’Connell 1991; Bradstock et al. 1992; Bell 1994).Although this means that the seed bank is not likely tobe depleted following any one fire, it might also furtherreduce the size of the recruiting cohort in the smallseeded species relative to larger seeded congeners.Regardless of size, seeds buried too close to the soilsurface (e.g. 0–2 cm) may also receive lethal temper-atures (>120�C; Auld & O’Connell 1991) during hotfires. Mucunguzi and Oryem-Origa (1995) found thatthe majority of Acacia sieberiana seeds stored in the soilwere killed at a soil temperature of 120�C. Seeds mayalso perish because of prolonged temperature and/orwater stress if buried too close to the soil surface (Tozer1998).

Although the results for rare versus common specieswere consistent with expected patterns in relation toseed size and emergence, results for other seed-basedtraits were inconsistent. Heat treatments revealed thatone of the rare species, A. ausfeldii, showed almost noincrease in germination until seeds were heated to100�C for 5 min. Failure of the low and intermediateheat treatments to break seed dormancy suggests thatonly a narrow window of temperatures associated withsoil heating by fire might prove suitable for recruitmentin this rare species. More specific fire-related cueing ofgermination means that variations in fire intensity andevenness will limit the chances for successful recruit-ment so that the species can only occupy a small partof the landscape. This factor alongside an apparentrestriction of seedling recruitment to shallow soildepths (Fig. 3) could restrict population size andspread in this species. The other rare and commonspecies tested here showed patterns of heat stimulatedgermination that were not consistent with the hypo-thesized relationship of narrower requirements inrare species. Nevertheless, the most common andwidespread species tested, A. pycnantha, showed thebroadest response to heat treatments, with high ratesof germination across temperatures from 60 to 100�C.

Rare species characterized by small population sizehave been reported to produce fewer seeds per plantthan common congeners, and to show higher variationin levels of seed set within populations. This is generallyinterpreted to be a consequence of small-populationeffects on fecundity, including pollinator limitation,

self-incompatibility and inbreeding depression. Forexample, Kery et al. (2000) reported reduced seed setin small populations of the self-incompatible grasslandperennials Gentiana lutea and Primula veris, as didOostermeijer et al. (1998) for the rare perennial,Gentiana pneumonanthe. In this last case greater vari-ation in reproductive success was also observed amongindividuals in smaller populations. Cunningham(2000b) found that seed set efficiency decreased withfragment size in Acacia brachybotrya in mallee wood-lands of central New South Wales and concluded thatthis was a consequence of declining pollination becausepollen supplementation increased seed set. Giblin andHamilton (1999) and Brown and Kephart (1999)similarly concluded that pollination limitation was themain cause of low seed set in rare Aster and Silenespecies, respectively.

In the present study, where populations ranged fromsmall to medium in size, variation in seed productionamong individuals within a population was the highestfor the rare species A. williamsonii (CV = 3.15), butwas equally low for both a rare (A. ausfeldii) and acommon (A. paradoxa) congener (both close to 1.0).Equally ambivalent results were observed for total seedset where seed production was highest for one of therare species (A. ausfeldii) and lowest for the mostcommon species (A. pycnantha). Nor did rare specieshave higher levels of seed abortion or lower seedviability than common species. However, substantialvariation among three populations for levels of heattriggered germination in A. ausfeldii (12–38%) wasrecorded. Again, not all populations of the rare specieswere small; although many populations are small, rarityin A. ausfeldii and A. williamsonii may be due more torestricted distribution and habitat than small popu-lation sizes. In order to test the potential role of pollin-ation limitation and other genetic factors on seed setand viability, a range of populations of different sizesneeds to be sampled, and self- and crossed-pollensupplementation tests conducted.

Although it is not possible to accept the contentionthat rare species in general will show lower seed pro-duction and greater variance in seed set within popu-lations due to small-population effects, the explanationmay nevertheless be relevant to the expression of rarityin A. williamsonii. On-plant granivory was highest forthe rare species, A. williamsonii, and overall reductionin potential seed set due to the combination of incom-plete seed development and granivory was also highestin this species. However, A. ausfeldii showed good seedset and little loss to on-plant granivores. Overall, thelevels of granivory did not appear sufficient to repre-sent a mechanism that might help to explain rarity inthese species.

Many factors that may be important in determiningthe rarity of the two Acacia species reported hereremain to be investigated. Murray et al. (2001) con-

SEED PRODUCTION AND GERMINATION IN ACACIA 279

sidered the role of rhizobial symbionts in the distri-bution of three restricted and three widespread easternAustralian Acacia species, but found no clear evidenceto support the contention that symbiont specificity andavailability of N-fixing symbionts might be a deter-minant of species distributions and abundances onnutrient-poor Australian soils. A similar question couldbe asked in relation to mycorrhizal associates andphosphorus nutrition. The present study focused onseed production, viability and recruitment, but did notexplore plant pollination biology, so that we have noinformation on levels of self- versus out-crossing andthe effectiveness of pollen from near versus distantneighbours. Demographic data remain to be collectedconcerning age at reproductive maturity, and year-to-year and site-to-site variations in seed production,especially in relation to population sizes and densities.Similarly, survival of seedlings and juveniles to matur-ity, length of reproductive period and reproductiveschedules in general remain to be investigated. Finally,environmental attributes of habitat have not been fullysurveyed, and a more complete analysis of habitatcircumstances might reveal specific habitat require-ments. These areas are the subject of continuing study.

ACKNOWLEDGEMENTS

This study was funded as part of an ARC-Industry(SPIRT) grant to N. J. Enright for research into theecology of the box–ironbark ecosystem of centralVictoria. We acknowledge the support of our industrypartner, the Department of Natural Resources andEnvironment, Victoria, and of Parks Victoria for theirco-operation in issuing the required permits for collec-tion of samples from rare flora. Yvonne Buckley, WillEdwards and Michael Bull provided helpful commentson an earlier version of the manuscript.

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