Journal of Ecology (1990), 78, 113-133

PHENOLOGICAL TRENDS WITH LATITUDE IN THEMANGROVE TREE AVICENNIA MARINA

N. C. DUKE*

Australian Institute of Marine Science, Townsville, Queensland, Australiaand James Cook University of North Queensland, Queensland, Australia

SUMMARY

(1) Leaf fall and reproductive phenology of Avicennia marina assessed during 1982-83using litter fall collections from twenty-five sites in Australia, Papua New Guinea and NewZealand revealed major trends with latitude. Flowering shifted from November-December in northern tropical sites, to May-June in southern temperate sites. Periodsbetween flowering and fruiting increased from two to three months in tropical sites to tenmonths in southernmost sites. Leaf fall was more variable with unimodal annual peaks intemperate sites and often multimodal patterns in the tropics.

(2) Correlative evaluation of simple models suggested that initiation of the reproductivecycle occurred when daylength exceeded 12 h, followed by rates of development toflowering and fruit maturation given by a linear function of mean daily air temperature.This explained up to 92% of variance in total cycle duration and timing. Temperatureaffected reproductive development by increasing growth rates by a factor of two or threefor each 10º C rise. The model was tested using independent data to predict timing ofreproductive events in respective sites.

(3) Appearance of new leaves on canopy shoots in situ near Townsville, northernQueensland, had seasonal highs followed by peak falls a month later, and leaf longevitywas estimated to be around thirteen months. Timing of new leaf appearance and leaf fallwere comparable with observations from other studies and sites, geographicallyoverlapping with the present litter-fall sites in Australasia. These had seasonal peaks,chiefly related to either the reproductive cycle during initiation of inflorescencedevelopment or independent growth. Respective heights of these peaks for particular sitesappeared to depend on environmental factors of temperature and moisture. Thus,inflorescence leaf appearance was predominant in low-moisture and low-temperature sitesduring early summer, and independent leaves appeared mostly in wetter tropical sitesduring winter months.

(4) Distributional limits of A. marina in higher latitudes coincide with trends towardszero reproductive success (notably seen in flowering). This was apparently brought aboutby a convergence of phenological events within the shorter growth period of summer inthese latitudes.

INTRODUCTION

The mangrove tree Avicennia marina (Forsk.) Vierh. sensu lato (Tomlinson 1986) iscommon throughout the Indian and Pacific areas, and occurs over a latitudinal rangefrom 30°N to 38ºS. Its range, apparently, is limited by low temperature (Macnae 1966)but this had not been substantiated. For Australasia (Australia, New Guinea, NewZealand and south-western Pacific), a relationship between temperature and distributionwas discussed by Saenger & Moverley (1985) based on leaf production phenology incentral Queensland. These authors found good agreement in their model for the southernlimit of the species, but curiously predicted its absence in northern Australia, Papua NewGuinea (P.N.G.) and other equatorial regions where it occurs. Work on additional species

* Present address: Smithsonian Tropical Research Institute, Balboa, Republic of Panama.

113

114 Phenology of Avicennia marina

of Avicennia had also failed to identify major factors determining vegetative andreproductive phenologies (e.g. Lopez-Portillo & Ezcurra 1985). In such cases, correlativeanalyses were restricted by the geographical limitations of their sample sets.

Data on phenology of Avicennia species were uncommon, but available reports ofphenological events (peak leaf appearance, leaf fall, flowering and fruiting) suggestedmajor differences in A. marina throughout Australia. For example, fruit matured duringFebruary and March in most years (Attiwill & Clough 1978) in Westernport Bay,Victoria, and Missionary Bay, northern Queensland (Duke, Bunt & Williams 1984); bycontrast, in the Brisbane River of southern Queensland, fruit matured in August (Davie1982). In another example (Semeniuk, Kenneally & Wilson 1978), flowering in WesternAustralia was observed to shift from November-January in northern sites to March-April in the south.

Interpretation using these data was further complicated by the current uncertainty inthe systematics of Australasian Avicennia (Tomlinson 1986; Duke 1988b, c). For instance,the most common taxon, A. marina, could include several species or forms which mayhave different phenological patterns. Data on vegetative and reproductive phenology(e.g. Attiwill & Clough 1978; Semeniuk, Kenneally & Wilson 1978; Wium-Andersen &Christensen 1978; Woodroffe 1982; Davie 1982; Duke, Bunt & Williams 1984) weretherefore insufficient to discriminate between clinical trends with latitude (or otherenvironmental gradients), and taxonomic subgroupings, or a combination of both.

However, two important patterns emerged from these data (also note Steinke &Charles 1984; Woodroffe et a l . 1988). First, there was considerable annual variation in thequantity of both flowers and propagules produced. Second, there was minimal year-to-year variation in the timing of events at any single site. This annual re-occurrence ofphenological events was considered site specific, but it was not known whether thisresulted from environmental or genetic differences. Therefore, a regional litter-fall studyby the Australian Institute of Marine Science (unpublished, included sites in NewZealand, Papua New Guinea and Australia) provided a rare opportunity to assess morefully the phenological behaviour of A. marina sensu lato over a wide geographic range.This evaluation had two objectives: first, to describe any patterns for phenological events;and secondly, to identify possible causal factors and develop a phenological model usingcorrelative techniques.

METHODS

Australasian study sites and litter-fall results

Sites were established under tree canopies of A. marina sensu lato at twenty-threelocations in Australia, one in New Zealand and one in southern Papua New Guinea(Table 1, Fig. 1). Two collection traps (each about 1 m2) were installed in most sites andresults were pooled for each site in analyses. Litter sites were visited monthly from August1982 to September 1983, and material sent to the Australian Institute of Marine Science(AIMS). Otherwise, collection, sorting and component classification followed earlierstudies (e.g. Duke 1988a). Briefly, litter was divided into four classes: leaves, wood, debrisand reproductive parts (AIMS, unpublished). The latter were further partitioned asflower bud primordia, immature buds, mature unopened buds (including flower budswithout corollas), full flowers, separate flower corollas, immature fruit and mature fruit.The term ‘corolla’, as used in this study, refers to the four fused triangular petal lobes, and‘fruit’ refers to the cryptoviviparous propagules which mature at abscission.

N. C. DUKE 115

TABLE 1. Study sites maintained during 1982-83 in the Australasian region (Fig. l),and helpers (including institutional affiliations, if any) who collected litter fall.

LatitudeS

9º32’

Site name

1 Port Moresby, P.N.G.

Jacky Jacky Creek, Qld

3 Darwin, N.T.

Weipa, Qld

Wyndham, W.A.

Cooktown, Qld7 Daintree River, Qld

Mornington Island, Qld

Cairns, Qld

Broome, W.A.

Hinchinbrook Island, QldChunda Bay, QldPort Hedland, W.A.

Dampier, W.A.

Exmouth, W.A.

Carnarvon. W.A.

LongitudeE

Volunteer collectors(institutional affiliation)

147ºl7’

Siteno.

G. Leach and M. Kuduk(University of P.N.G.)

R. Williams (Department of Aboriginaland Islander Affairs, Qld)

R. Hanley (Museums and ArtGalleries of the N.T.)

A. Gunness (ComalcoAluminium Co.)

W. Cox and C. Glover (Departmentof Agriculture, W. A.)

P. TimmermansW. StarckR. Coles (Qld Fisheries Service)

and Mornington Shire CouncilB. van Montfrans and R. Coles

(Qld Fisheries Service)

2 10°57’ 142º28’

12º21’ 130°57'

12º36’ 141°54'4

5 15º22’ 128º23’

15º28’ 145ºl5'16º17’ 145º20’16º42’ 139ºl3’

6

8

9 16º57’ 145º47'

10

111213

17º58’ 122º15’

18º15’ 146º14’19ºl7' 147º02’20º20' 118º25’

J. Looby, N. Sarti and R. K. Sutton(Department of Fisheries and Wildlife. W.A.)

author (Australian Institute of Marine Science)author (Australian Institute of Marine Science)T. Rose (Mt Newman

Mining Co., W.A.)14

15

16

20°44’ 116º37’

21’57’ 113º56'

24º28’ 113º41’

C. Nicholson (Department of Conservation and theEnvironment, W.A.) and Dampier Salt Co.

R. Taylor (National ParksAuthority of W.A.)

K. Marshall and J. Wilson(Department of Fisheries and Wildlife, W.A.)

J. Hughes (Griffith University, Qld)T. Blackman (N.S.W. State Fisheries)

and W. Allaway (Sydney University, N.S.W.)R. Wilkinson (N.S.W. State Fisheries)

and W. Allaway (Sydney University, N.S.W.)D. Smith and J. Williams (Department of

Conservation and Environment, W.A.)W. Allaway (Sydney University, N.S.W.)J. Johnston and M. M. Retallick

(Department of Fisheries, S.A.)C. Woodroffe and P. Crossley

(University of Auckland, N.Z.)C. Woodroffe and P. Crossley

(University of Auckland, N.Z.)A. Mundy (N.S.W. State Fisheries)

and W. Allaway (Sydney University, N.S.W.)P. Attiwill (University of Melbourne, Vic.)

17 N. Stradbroke Island, Qld 27º28' 153º25’18 Nambucca River, N.S.W. 30°42' 152º57’

19 Port Stephens, N.S.W.

Bunbury, W.A.

Botany Bay, N.S.W.Port Gawler, S.A.

Tuff Crater, N.Z.

Schnapper Rock, N.Z.

Merimbula, N.S.W.

Westernport Bay, Vic.

32º40’ 151°59’

20

2122

23a

23b

33º20' 115º39'

34º0l’ 151º09'34º42’ 138º28'

36º48’ 174º45'

36º48’ 174º45'

24

25

36º54 149º53'

38º21’ 145º13'

Localized studies of within-site variation in phenology

Shoot growth and litter fall of A. marina were monitored together at Blacksoil Creek,near Chunda Bay (site 12), from July 1986 to September 1987 to investigate within-sitevariation, and the relationship between leaf appearance and leaf fall in one site. Littercollection was conducted as described above except that collections were madefortnightly. Eight traps were installed, with four each in high and low intertidal positions(representing extremes of habitat in this site); results are presented in Duke (1988c). As nosignificant differences were found between traps, results were pooled. Similarly, results

116 Phenology of Avicennia marina

FIG. I. Litter-fall collection sites during the 1982-83 study of hicemziu murina in the Australasianregion (numbered sites described in Table I).

were also pooled from shoot observation sites (Duke 1988~). These consisted offortnightly scores of new leaves, leaves lost, reproductive part counts and status, andnumber and position of new apical shoots. Six trees were monitored, with three each inhigh and low intertidal positions. For each tree, at least twenty leafy crowns (six to tenleaves each) were chosen from throughout the canopy.

Another aspect of phenological variation between sites, but within one location, wasassessed briefly in the estuary of the Murray River, Queensland (1805’S 146’Ol’E, nearsite 11) where there was considerable up-river salinity variation (Duke 1984). This survey,conducted in January 1987, consisted of scoring reproductive status (as numbers anddevelopmental stage of flower buds inflorescencee’) for trees of A. murina in at least threelow intertidal trees at each of five up-river sites, from the river mouth to their furthestextent of the species upstream. These results were consistent with little or no variationbetween sites within one location.

Interpretative and analytical procedures

On the basis of past experience, fall of flowers or fruit was indicative of flowering orfruiting (propagule maturation), respectively (e.g. Duke, Bunt & Williams 1984). Shootand litter-fall studies at Blacksoil Creek also confirmed this observation. Phenologicalevents were defined as respective periods of maximal leaf appearance, leaf fall, floweringand fruiting. Phenophases were defined as the periods between two such events, notably inthe reproductive cycle.

The annual re-occurrence of the phenological events was a basic assumption in thisstudy. The evidence for this came from several longer-term studies at specific locations(notably Steinke & Charles 1984; Woodroffe et uZ. 1988; also Table 6). However, amountsof reproductive material were expected to vary from year to year; therefore, all referencein quantitative considerations to full (or complete) reproductive cycles refer only to those

N. C. DU K E 117

Siteno.

6789

10111213141516171819202122232425

TABLE 2. Mean and maximum daily temperatures (month indicated by number;1 = January, 2 = February, etc.) and annual rainfall for sites of Australasian litter

collection in 1982-83, and respective averages over at least ten years.

Site name Minimum

1 Port Moresby, P.N.G.2 Jacky Jacky Creek, Qld3 Darwin, N.T.4 Weipa, Qld5 Wyndham, W.A.

Cooktown, QldDaintree River, QldMornington Island, QldCairns, QldBroome, W.A.Hinchinbrook Island, QldChunda Bay, QldPort Hedland, W.A.Dampier, W.A.Exmouth, W.A.Camarvon, W.A.N. Stradbroke Island, QldNambucca River, N.S.W.Port Stephens, N.S.W.Bunbury, W.A.Botany Bay, N.S.W,Port Gawler, S.A.Auckland, N.Z.Merimbula. N.S.W.Westernport Bay, Vic.

Mean daily temperatures (ºC)

1982-83 (month)Maximum

24.7 (8)24.2 (8)24.0 (7)23.9 (7)23.1 (7)20.9 (7)21.8 (8)20.0 (7)19.8 (7)20.2 (7)17.7 (7)19.8 (7)20.1 (7)19.4 (7)16.8 (7)15.4 (7)15.6 (7)13.3 (7)12.6 (7)12.6 (7)11.8 (7)9.9 (7)

10.4 (7)9.4 (7)9.8 (7)

29.0 (12)28.9 (12)29.6 (1)29.1 (1)33.7 (12)29.0 (1)29.3 (1)30.0 (1)28.3 (1)30.9 (12)28.5 (1)28.1 (1)31.4 (2)32.2 (2)31.1 (2)27.4 (3)25.5 (2)23.5 (3)23.3 (2)22.7 (1)24.1 (2)24.2 (2)19.0 (3)21.3 (2)23.4 (2)

Average (month)Minimum Maximum

25.1 (7) 28.2 (11-12)24.8 (7) 29.2 (11)24.6 (7) 28.9 (11)23.9 (7) 33.0 (11)22.4 (7) 27.9 (12-1)22.8 (7) 28.6 (1)20.6 (7) 29.5 (12)21.3 (7) 27.4 (1-2)21.2 (7) 30.2 (12)19.7 (7) 27.1 (1)20.1 (7) 27.8 (12)19.4 (7) 30.8 (1)19.8 (7) 31.3 (2)17.6 (7) 31.1 (2)16.6 (7) 27.8 (2)15.0 (7) 25.1 (1)12.8 (7) 23.0 (1-2)12.5 (7) 22.4 (1)12.6 (7) 21.6 (2)12.0 (7) 22.1 (1-2)10.9 (7) 21.9 (2)

9.9 (7) 20.2 (2)9.5 (7) 20.0 (2)

Rainfall (mm)annual total

1982-83 Average

54112491664151073201177205310181723688

1976988281

37109163

148018441147714

1295489794618493

171416631851774

2021248513992034

58121811097314255212232

118617191125800

1271459

813652

which were monitored from beginning (first appearance of immature buds) to end (fruitmaturation/abscission) in litter-fall studies.

Estimates of flowering and fruiting success, fruit set, and incidence of abortion forrespective components (notably in Fig. 9) were calculated as follows. Reproductivecomponents were collectively called ‘units’ because of the potential they represent in a life-history progression. The total number of these units (Σ immature buds + maturebuds + flowers + immature fruit + mature fruit), fallen during at least one complete cycle,would make up the putative original number of immature buds on the tree at thebeginning of the cycle. Percentages of units were then computed for respectivedevelopmental stages. For example: (i) flowering success was calculated as the percentageof total units which fell as flowers or fruit (i.e. Σ flowers + immature fruit + mature fruit);and, (ii) fruit set was calculated as the percentage of fruit units (Σ immature fruit + maturefruit) to original flowers.

Physical data

Records of rainfall and temperature were obtained from the Australian GovernmentMeteorological Office Stations (see Fig. 3) nearest to sites of litter collection (Table 2).These data were averaged for the collection periods at each site. Periods of relatively highevaporation and rainfall were derived from specifically scaled, matched annual plots ofmonthly temperature and rainfall (described by Walter & Leith 1967). For example, atCape Cleveland meteorological station (in the vicinity of Blacksoil Creek and ChundaBay study sites) in 1986-87 (Fig. 2), high evaporation was assumed to be important during

118 Phenology of Avicennia marina

-7 4

0TJ 35

E3 30

2

0

.G 25 ;

!F 20I

a

15 F$J

0A S O N D J F M A M J J

10

(b)

1986 I987

A S O N D J F M A M J JI986 I987

FIG. 2. Climatic records for the nearest meteorological station to Blacksoil Creek study site inQueensland Cape Cleveland, 19º l l’S, 147º0l’E) during 1986-87: (a) fortnightly plots of meandaily rainfall ( ) and mean daily temperature (- ) ; (b) a derived monthly bar chart ofperiods where temperature exceeds rainfall (i.e. periods of high evaporation; H), and rainfall

exceeds 3.3 mm day-1 (wet season months; x).

the months of August, January and February (where, in the plot, temperature exceedsrainfall), and rainfall was high during the months of January and February (where rainfallexceeds 3.3 mm day-1, or c. 100 mm calendar month-1; the acknowledged ‘wet’ season).Similar criteria were used to describe twenty-five meteorological stations in the vicinity ofAustralasian litter-fall sites during 1982-83 (Fig. 3). Irradiance (PAR-for cloudlessskies), solar angle (measured from the horizon) and daylength (time between actualsunrise and sunset) at each site and period were calculated using standard parameters.Estimates were similar to those obtained in tables (Walton Smith 1974). Statisticalprocedures followed Sokal & Rohlf (1981).

Regression models

Relationships between the phase duration (the inverse of rate of development) for twophenophases (pre- and post-anthesis) and mean daily temperature and mean dailyphotoperiod, were examined by fitting several regression models (Table 3). In the models,duration (D) was used because this estimate represents the inverse transformation ofdevelopment rate, a transformation commonly used when testing rate variables. Modelswere compared for goodness of fit using increase in explained variance and reduction ofresidual mean squares.

Models T, P, T, P, TP and T, P,TP represent standard linear regression relationshipswith various combinations of the independent variables and interaction terms. Models T2

and TP2 are second-order polynomials. These were included to help describe anytemperature optima; hence they were not used on results for photoperiod. Moreexhaustive assessment of results (not reported here) confirmed this view. All models weretested if they had ‘biological sense’. Earlier crop studies have demonstrated similarrelationships between mean daily air temperature and mean photoperiod (e.g. Perry,Siddique & Wallace 1987)

N. C. DUKE 119

1 Port Moresby, P.N.G.

2 Thursday Island, Qld

3 Darwin, N.T.

4 Weipa, Qld

5 Wyndham, W.A.

6 Cooktown, Qld

7 Low Isles, Qld

8 Mornington Island, Qld

9 Cairns, Qld

10 Broome, W.A.

11 Cardwell, Qld

12 Cape Cleveland, Qld

13 Port Hedland, W.A.

14 Karratha, W.A.

15 Learmouth, W.A.

16 Carnarvon, W.A.

17 Brisbane, Qld

18 Coffs Harbour, N.S.W.

19 Newcastle, N.S.W.

20 Bunbury, W.A.

21 Sydney, N.S.W

22 Adelaide, S.A.

23 Auckland, N.Z.

24 Merimbula, N.S.W.

25 Melbourne,Vic.

FIG. 3. Monthly bar chart plots of periods of highest evaporation (<) and wet season months ( x )for meteorological stations nearest to sites of Australasian Avicennia marina litter collection

during 1982-83. Sites are ordered by latitude south.

Model A in Table 3 represents a form of the Arrhenius equation of chemical reactionkinetics (Latham 1962). This model was included in view of the relationship betweenchemical reaction rates and temperature (the latter being a function of latitude).

RESULTS

Interpretation of phenological information

Interpretation and construction of phenograms followed methods established earlierfor other mangrove genera (Duke, Bunt & Williams 1984; Duke 1988a). Thus, for A.marina these were derived from serialized plots of numbers of reproductive componentsof litter fall. Of the twenty-five sites, four widely separate examples (Fig. 4) are describedin detail; Port Moresby, Papua New Guinea (site l), Trinity Inlet near Cairns, Queensland

120 Phenology of Avicennia marina

TABLE 3. Models used to test the relationship between temperature and/orphotoperiod to explain reproductive growth periods. D represents the duration ofthe phase (days); TM, TA and PM the mean daily temperature (ºC), absolutetemperature (ºK) and mean photoperiod (h); and b0, b1, b2 and b3 fitted regressioncoefficients. Note that phase duration is the inverse of the daily development rate.

Name Development model

T D=b0+b1(T M)T2 D=b 0+b1(TM)+b2(TM)2

P D=b0+b1(PM)T,P D=b0+b1(TM)+b2(PM)TP D=b0+b1 (TMxPM)TP2 D=b0+b1(TM)+b2(TMxPM)2

T,P,TP D=b0+b1(TM)+b2(PM+b3)(TMxPM)A -ln( l /D )=b l(103/TA)-b0

(site 9), Carnarvon in Western Australia (site 16), and Port Gawler near Adelaide, SouthAustralia (site 22).

In Port Moresby (Fig. 4a) fall of leaves occurred over three months in winter. Immaturebuds were first observed in the litter in October 1982 and flowering peaked in December.This represented a period of about two months to anthesis. Falls of mature fruit occurredshortly after, mostly in February 1983. Thus, post-anthesis development took approxi-mately two months, and the total reproductive cycle occurred during the summer period.

At Cairns (Fig. 4b) A. marina behaviour was similar to that briefly noted (Duke et al.1984) in north-eastern Australia. Leaf fall was erratic, but highest during winter monthsand lowest in summer (December-January). Peak flower fall was better defined, occurringin December 1982, nearly two months after immature buds were first observed in Octoberlitter. Mature fruit fall occurred chiefly in February and March 1983. Thus, the timebetween flowering and maturation of fruits was approximately three months, and treeswere devoid of reproductive material for the rest of the year.

Carnarvon (Fig. 4c) differed from more northern sites by having a predominantlysummer leaf fall, peaking in November 1982. Immature buds were also much later, firstobserved in January 1983. Flowering peaked in February, just one month later. Falls ofmature fruit occurred in winter, peaking in May 1983. Post-anthesis developmenttherefore occurred over three months.

In Adelaide (Fig. 4d) the trees had a summer leaf peak fall near January and February,1983. Immature buds and flowers fell in February and mature fruits fell in December, i.e.ten months from flower to propagule fall. This was estimated by substituting 1982-83results of mature fruit fall in the next year, assuming annual re-occurrence of phenologicalevents as discussed in the methods.

Geographic clines in flowering and fruiting

Phenograms (similar to those in Fig. 4) for other sites were not presented becausetiming of peak falls followed simple and consistent patterns for most components. Thiswas particularly evident for major reproductive events of flowering and fruiting in respectto latitude (Fig. 5).

Flowering occurred progressively later in higher latitude sites with a relationship thatwas virtually linear (r2 = 0.834, n = 25, P < 0.001). Thus, in northern sites (c. 10°S)flowering occurred during November and December, and progressively shifted six

N . C . D U K E 1 2 1

ta) 30- 20 - leaves

IO - I l L ! / h l

IL

immature buds

mature buds mature buds

3 2 immature fruit

_ lk

: 4 mature fruit 2

ki 0

z ASONDJFMAMJJASO

flowers

I I I I I I I 1

2- immature fruit l-

o?J ’ ” ’

~ ~ l l l , l ~ ~ ~ ~ ~ ~ t ASONDJFMAMJJASO

immature buds

flowers

I I I 1

0 ” “ “ ” ASONDJFMAMJJASO ASONDJFMAMJJASO

l982- I983

F I G . 4. P h e n o g r a m s f o r Auicemiu murinu, d e r i v e d f r o m l i t t e r - f a l l c o l l e c t i o n s d u r i n g 1 9 8 2 - 8 3 a t f o u r A u s t r a l a s i a n s i t e s : ( a ) P o r t M o r e s b y , P a p u a N e w G u i n e a ( 9 O 3 2 ’ S , 1 4 7 ’ 1 7 ’ E ) ; ( b ) C a i r n s , Q u e e n s l a n d ( 1 6 % “ S , 1 4 Y 4 7 ’ E ) ; ( c ) C a r n a r v o n , W e s t e r n A u s t r a l i a ( 2 4 O 2 8 ’ S 1 1 3 ’ 4 l ’ E ) ; a n d , ( d ) A d e l a i d e , S o u t h A u s t r a l i a ( 3 4 ’ 4 2 ’ S 1 3 8 “ 2 8 ’ E ) . T h e p h e n o g r a m s d e m o n s t r a t e g e o g r a p h i c

c l i n e s i n p h e n o l o g i c a l e v e n t s .

122 Phenology of Avicennia marina

CA m-º

2 ix..z

53 0 -

;n x <

❑ X❑ i

< ;

❑ ❑❑ ; **

❑ x X❑ : X

;D <<

,,,,,,,,,,,,,,,,,,,,,,40 A S O N D J F M A M J J A S O N D J F M A

I I1982-83 substituted

FIG. 5. Reproductive and phenological events in Avicennia marina for one full cycle observed inAustralasian litter-fall studies during 1982-83: first immature buds (❑); flowers (x); and maturefruit (<). The latter seven months for seven higher-latitude sites, shown for 1983-84, were

substituted from 1982-83 results (see text).

months to May and June in southern sites (c. 38ºS). This result compared favourably withthe observations of Semeniuk, Kenneally & Wilson (1978).

Peak fruit maturation also shifted, but the range was greater (extending over a full year)and the relationship with latitude was clearly non-linear. A marked change occurredabout the Tropic of Capricorn (around 23º2’S). In the tropics, fruit fall (in March andApril) followed two to three months after flowering, but in higher latitudes this periodprogressively increased to nine months, i.e. to February of the following year.

In this study, it was convenient to consider two major phases within the reproductivecycle. The most obvious was the period between flowering and fruiting, termed post-anthesis. The other was pre-anthesis, or the period from an estimated initiation date of thereproductive cycle to flowering. Evidence of initiation was shown in the litter by the firstappearance of immature buds. This was therefore taken as the first estimate of initiationdate, occurring in most Australasian litter-fall sites in October and November (Fig. 5).Furthermore, concurrent shoot observations and litter collections at Blacksoil Creek nearsite 12, supported the idea of using such litter-fall results to interpret current canopyphenology. In summary, results of Australasian litter studies, expressed using these twomajor phases, clearly showed further latitudinal trends where duration of each wasincreased in higher-latitude sites.

Trends in the appearance and fall of leaves

Before investigating Australasian trends in leaf-growth phenology, it is helpful toconsider the relationship between leaf appearance and fall. Appearance of new leavesgenerally preceded leaf fall by about one month (with leaf longevity around thirteenmonths), based on shoot studies at Blacksoil Creek in 1986-87 (Fig. 6). In this case, bothappearance and fall of leaves were disproportionately bimodal, with comparable lesser(around 50%) peaks in September and October 1986, and major peaks in February-March and March-April 1987, respectively. Furthermore, leaf-fall estimates from shootobservations (Fig. 6) were compared with corresponding litter-fall studies at BlacksoilCreek (r2=0.622, n =25, P< 0.00l) , suggesting that leaf-fall results may be used toextrapolate trends in leaf production for this tropical site. Similarly, the relationship was

N. C. DUKE 123

E 6-2z 4

5= 2z

3 0A S O N D J F M A M J J A A S O N D J F M A M J J A

I986 1987 I986 I987

01’| | | | | | | | | | | | | | |A S O N D J F M A M J J A

I986 1987

FIG. 6. The relationship between leaf appearance and leaf fall (numbers of leaves) in litter-fall andshoot studies of Avicennia marina at Blacksoil Creek, Queensland (1986-87). Shoots (> 120) werechosen from throughout the canopy in six trees, measuring (a) leaf appearance and (b) leaf loss/fall, while (c) leaf fall was sampled concurrently from eight nearby litter-fall traps. Bars representestimates of standard error. The apparent co-ordination of leaf appearance one month before fallwas tested by systematically calculating shifted correlation estimates between appearance and fallin shoot observations. The value of greatest significance (r2 = 0.623; n =23; P <0.001) wascalculated when leaf-fall results were shifted back against leaf appearance by two collection

periods, i.e. one month.

used in a much wider context because it compared well with other Australian field studies(e.g. Attiwill & Clough 1978; Davie 1982; Saenger & Moverley 1985). These findingstherefore suggested that leaf-fall peaks may be interpreted as flushes (or peak appearance)of new leaves in the previous month.

In this Australasian study, leaf fall appeared to be related to latitude (Fig. 7), but therelationship changed between sites in an apparently irregular way. In temperate andsubtropical sites (sites 16 to 25) maximal leaf fall occurred in summer although there was amarked shift to earlier months (around October) in more northern sites. Patterns intropical sites were more difficult to interpret, but there was a tendency for major winter(June-July) peaks of leaf fall; note for Port Moresby (site 1). However, there was also atendency toward apparently erratic, or multimodal, phenological patterns. These maybest be considered multimodal, because of the evidence of annual replication of overallpatterns discussed earlier. For example, the bimodal pattern observed at Chunda Bay(site 12) was seen in both study periods (1982-83 and 1986-87; compare Figs 6 and 7), aswell as in a previous study (Saenger & Moverley 1985) over several years (1979-82) on the

124 Phenology of Avicennia marina

Australian east coast at Proserpine (20º30’S) and Gladstone (23º50’S). Meanwhile theunimodal pattern for temperate sites in this study was also observed by Davie (1982) at asite comparable to site 17.

DISCUSSION

Reproductive-cycle development

The relatively simple patterns observed in reproductive events suggested that control ofthis phenology was influenced by a small number of factors. Thus, timing of firstappearance of immature buds, flowering and fruiting events, which clearly followedlatitudinal clines, displayed little or no variation due to localized influences such asrainfall, evaporation, salinity, nutrients, and so on. For example, sites along the generallyarid west coast of Australia (sites from 20º to 25ºS in Fig. 5) compared favourably withthose on the wetter east coast (most other sites). Causal factors were therefore expected tobe related to latitude, provided that differences between them were environmentallyinduced rather than inherited. The notion of a phenetic basis to this variation was alsosupported by preliminary observations during growth studies at the Australian Instituteof Marine Science (unpublished), where immature buds and flowers appeared syn-chronously in transplants from several Australia-wide locations (equivalent to sites 3, 7,11, 17 and 21). Causal factors could have influenced the timing of phenology in at leasttwo major ways: first, they may act as triggers for initiation or intermediate events such asflowering; secondly, they may influence developmental rates between phenologicalevents. This study assessed these aspects by considering the reproductive cycle in twoparts; pre- and post-anthesis.

Possible causal factors-pre-anthesis development and initiationIt was unlikely that causal factors acted as direct threshold stimuli to flowering because

timing of flowering was not directly related to latitudinal factors such as temperature,photoperiod or irradiance. However, it was likely that causal factors were related to pre-anthesis phenophase duration (inverse of daily development rate). Studies in crop growth(e.g. Perry, Siddique & Wallace 1987) demonstrated that temperature and photoperiodmay be used to predict phase duration in some plants. The present study tested similarmodels, and these results are summarized in Table 4. Using the maximal varianceexplained, the best-fit model for the initiation (first appearance of immature buds) toflowering phenophase, with 71.2%, was a second-order polynomial (model T2) basedsolely on mean daily temperature. The inclusion of photoperiod did not improve theresult.

This finding also provided a basis for determining which factors influenced reproduc-tive cycle initiation. Thus, because major shifts in flowering dates (Fig. 5) were explainedby temperature differences between sites, it followed that initiation would have a smallershift in time from north to south. If initiation preceded first appearance of immature budsby one or two months, and development rates were constant (acceptable in view of theearlier correlation), the trends for both first immature buds and flowering with latitude(temperature) may be extrapolated to indicate an environmental trigger. Of three possiblefactors related to latitude, only two had fixed (possible-threshold) values for each site.These preceded appearance of immature buds by a month or so. The first was solaraltitude at around 7 5 º above the horizon (= PAR noon irradiance of about 2101 µE m-2

S-1). This value was taken because it occurred over the full range of A. marina, and at the

125

3

4

567

8

9

10

11

12

13

14

A S O N D J F M A M J J A S

I982 I983

FIG. 7. Patterns of leaf fall in Avicennia marina (plotted separately as numbers of leaves m-2 day-1

in litter; compare with Fig. 4) at twenty-five Australasian sites (Table 1) ordered by latitude.Reproductive events: putative initiation (.......), flowering (❍), and fruiting (●).

Port Moresby, P.N.G

Jacky Jacky Creek, Qld

Darwin, N.T.

Weipa, Qld

Wyndham, W.A.Cooktown, QldDaintree River, QldMornington Island, Qld

Cairns, Qld

Broome, W.A.

Hinchinbrook Island, Qld

Chunda Bay, Qld

Port Hedland, W.A.

Dampier, W.A.

15 Exmouth, W.A.

16 Carnarvon, W.A.

17 North Stradbroke Island, Qld

18 Nambucca River, N.S.W.

19 Port Stephens, N.S.W.

20 Bunbury, W.A

21 Botany Bay, N.S.W.

22 Adelaide, S.A.

23 Auckland, ,N.Z

24 Merimbula, N.S.W.

25 Westernport Bay, Vic.

southernmost occurrence this took place on 22 December (the summer solstice). Innorthern sites this value occurred in early September. The second factor was daylength(photoperiod) increasing to just over 12 h (first long day) which occurred from early tolate September for sites from north to south, i.e. the period before the equinox on22 September.

The relative importance of these two factors was assessed by comparing the goodness offit for each model using their different estimates of phase duration. These were furthercompared with the ‘first-immature-buds-to-flowering’ model, described earlier. Resultsare presented in Table 4. Solar altitude was least favoured because the percentagevariance explained was much less in all models tested; this result was supported by theobservation of peak flowering in both shaded plants and unshaded plants nearby(personal observation). By contrast, daylength appeared to trigger initiation of the

126 Phenology of Avicennia marina

TABLE 4. Estimates of percentage variance for evaluation of models listed in Table3. Period durations (inverse of daily development rate) are estimated for pre-anthesis, post-anthesis and total phases including hypothetical initiation phases(see text) measured from time of (1) solar altitude greater than 75º (= an irradiancethreshold), and (2), daylength greater than 12 h. *P < 0.05; **P < 0.0l;

***P < 0.00l; N.S., not significant.

Phenophase T T2 P T,P TP TP2 T,P,TP A

First immature buds 31.1** 71.2*** 20.8* N.S. N.S. 44.2** 30.5* 28.2**to flowering

Putative initiation (1) 30.5** 56.3*** N.S. 30.6* 28.1** 56.4*** 57.0*** 28.7**to flowering

Putative initiation (2) 64.8*** 77.9*** 34.4** 66.0*** 60.0*** 74.8*** 74.8*** 56.4***to flowering

Flowering to mature fruit 88.2*** 91.7*** 27.9* 89.3*** 85.0*** 89.9*** 89.5*** 90.4***Putative initiation (2) - 92.7*** - - - - - 89.6***

to mature fruit

reproductive cycle. This was shown by an increase (from the ‘first-immature-buds-to-flowering’ model) in percentage variance explained (77.9%) in the daylength initiationtrigger, using the T2 model. In this model, phenophase duration decreased (i.e. dailydevelopment rate increased) when temperature increased, and a maximum developmentrate occurred around 28 ºC (Fig. 8a; T2 model). Above this temperature in the model,phenophase duration again increased, but this was not substantiated by present results.Other models included factors of photoperiod, various combinations, and interactionterms, but these were less important in the tests.

Temperature also appeared to affect success of flowering (i.e. numbers of flowers as apercentage of original immature buds; see Methods). This generally increased withaverage mean daily temperatures (Fig. 9) and a plateau around 70% flowering successcoincided with tropical latitudes and temperatures greater than 25 ºC. In temperatelatitudes approaching 35ºS, flowering success neared zero with mean daily temperaturesaround 18 ºC.

Possible causal factors-post-anthesis developmentPost-anthesis development rate decreased much more with latitude than the rate before

flowering (Fig. 5). In tropical sites fruiting shifted from February to April and maintaineda roughly constant development period of two or three months. In temperate sites thisshift was from April in one year to March in the next, representing a change in duration ofdevelopment from three months to around ten months.

The various models described earlier were also applied to post-anthesis phenophase.These tested the predictive importance of mean daily air temperature, photoperiod, orboth, for phenophase duration (the inverse of daily development rate) from flowering tofruiting. The T2 model showed exceptional results (explaining 91.7% of variance), but wasonly marginally better than the first-order (T) and the Arrhenius (A) models. Choice ofmodels at this point was somewhat arbitrary, but in view of the temperature-durationplot (Fig. 8b), the T model linear regression was considered less appropriate in describingthe results. Nevertheless, these findings show the importance of temperature indetermining rates of post-anthesis development.

Unlike flowering, fall of mature fruit showed no obvious relationship with latitude(Fig. 9a), temperature, or any other major climatic factors such as annual rainfall(compare sites in Fig. 9a and Table 2). Similarly, fruit set (i.e. the ratio of post-anthesis

N. C. DU K E 127

300 -

250 -

200 -

I50 -

I00 -

( a ) ‘ In i t iat ion’ to flowering

T2 model.Ll ... 8. ?l d .. .

.

A model

( b ) Flowering to mature frui t

( c ) 'Initiation' to mature fruit

T2 model 6.5~ A model

4 5 0 -

6.0 -

350 -

5.5 -2 5 0 -

I50 - ’ - ’ - ’ - ’ - ’ 5.0n * , 4

IO I5 20 25 30 35 3.2 3 .3 3 . 4 3 . 5

Temperature º C (Absolute temperature ºK)-1 x 103

FIG. 8. Regression plots for the best-fit models, T2 and A (described in the text and Table 3) fordevelopment rates in Avicennia marina (a) putative initiation to flowering; (b) flowering to

fruiting; and (c) putative initiation to fruiting.

units to original flower numbers; see Methods) was not related to latitude, and averaged10.4% (± 2.4% S.E.M.) for all sites. This implied that within-site or local climaticvariables played a greater role in determining fruiting success.

Predictive models of reproductive-cycle phenophases

The importance of the relationship with temperature in phase duration may be entirelydue to its effect on chemical reaction rates. It was generally observed that reproductive-cycle development rates doubled for each 10 ºC rise in temperature. This was further

128 Phenology of Avicennia marina

11 I2 I4 I5 16 I7 I8 I9 20

Sites ordered by latitude S

immature buds

mature buds

flowers

immature fruit

mature f ru i t

F IG. 9. (a) Percentages of reproductive components (immature buds, mature buds, flowers,immature fruit and mature fruit) of Avicennia marina in litter at some Australasian sites, usingresults for complete reproductive cycles only, during 1982-83 (i.e. those monitored from putativeinitiation to fruit maturation). The annual number of these reproductive units varied for each sitewith the original number ranging from 600 to 12 000 m-2. (b) Flowering success (percentage offlower numbers to original immature buds) in Australasian sites of A. marina as related to latitude

and to (c) mean daily air temperature.

supported by the success of the Arrhenius (A) model in explaining variance in phaseduration (Table 4, Fig. 8). The success of this model suggested that there was a particularsecond-order chemical reaction (activation energy, in pre- and post-anthesis phases,c. 2-3 kJ mol-1) acting to limit the daily development rate of the reproductive cycle. Thisnotion was not substantiated, however, and the A model did not explain an expectedreduction in rate for higher biological temperatures. This was suggested by the good fit ofthe second-order polynomial models (T2) and the apparent temperature optima around28 ºC. Growth studies are required to test these possibilities.

Nevertheless, both T2 and A models were useful predictors of phenological events forthis wide range of natural temperatures. Partial coefficients (with error terms andprobability estimates) of T2 - and A-model regressions for pre- and post-anthesisphenophases are presented in Table 5. Composite models are also presented in Table 4(plots presented in Fig. 8), covering putative initiation (daylength trigger) to fruiting. The

N. C. D U K E 129

TABLE 5. Partial coefficients of (a) best-fit regression models, and (b) the Arrheniusmodel (see text, and Table 4) for three reproductive phenophases including putativeinitiation (around the date when daylength becomes > 12 h, see text) to flowering,

flowering to fruit maturation, and putative initiation to fruit maturation.

Phenophase Coefficient

(a) Model T2 (D=b0+bl(TM)+b2(TM)2)Putative initiation to flowering b0

blb2

Flowering to mature fruit b0

blb2

Putative initiation to mature fruit b0

blb2

(b) Model A (-ln(l/D)=b1(103/TA)-b0)Putative initiation to flowering b0

blFlowering to mature fruit b0

b1Putative initiation to mature fruit b0

b1

Value S.E.M. t-Value Probability > t

888.6 148.1- 55.86 13.01

1.010 0.279738.9 119.8-43.92 11.73

0.725 0.2631518.4 226.2- 89.63 21.31

1.512 0.477

-11.101 2.941 - 3.774 0.0014.768 0.874 5.453 0.000

- 19.008 1.781 - 10.671 0.0007.046 0.527 13.365 0.000

- 15.544 1.650 - 9.423 0.0006.263 0.488 12.825 0.000

6.001- 4.295

3.6246.168

- 3.7462.7556.714

- 4.2073.170

0.0000.0000.0010.0000.0010.0130.0000.0000.005

predictive values of these models in estimating dates of events were assessed using two setsof independent data; namely, for A. marina in the same region but different years, and forA. marina in other regions. Predicted results (Table 6) were similar to observed dates,although bias was shown toward faster rates than predicted. There was no apparentreason for this, but collection-interval error is suggested to be partly responsible.Estimates might have been improved by using actual monthly mean daily temperaturesrather than year-to-year averages, as used in most cases due to availability of such data.Nevertheless, respective models appear to be relatively robust, despite both this and thewide geographic range of independent studies, particularly the site in South Africa.

Leaf appearance and fall

Possible causal factorsPrevious studies suggested that leaf growth in A. marina was optimal about 20 º C

(Davie 1982), and ceased at around 12 ºC (Saenger & Moverley 1985). These were notsupported by present evidence. The idea of growth cessation was briefly tested incorrelation calculations by excluding days in reproductive phase duration estimates whenmean daily temperatures were ≤12 ºC. Resulting correlations had lower levels ofpercentage variance explained than values discussed earlier. This suggested that growthwas continual, and that its rate was a simple function of temperature. There was noevidence of a temperature optimum.

Nevertheless, there were strong indications of temperature optima in annual leafappearance patterns for some groups of sites (Fig. 7). In temperate areas (sites 17-25), leafdevelopment was generally maximal when temperatures were at or near 20 ºC.Furthermore, in some tropical sites (sites 1, 4 and 5), leaf development was highest duringwinter months; the expected pattern for a 20 ºC optimum in sites where mean dailytemperatures never drop as low as this. However, this optimum model was a problem forintermediate tropical sites (notably sites 9-16) because these often had pronounced

130 Phenology of Avicennia marina

TABLE 6. Observed (o) and predicted (eT2, for model T2; eA, for model A; refer toTable 3) dates of phenoevents from independent data for ,4. marina in the sameregion but different years and for A. marina in other regions. Additional referencesources are indicated as footnotes. Mean monthly temperatures were taken, where

possible, from sources; otherwise average estimates were used.

Flowering date Fruiting date Fruiting dateSite ‘pre-anthesis’ ‘post-anthesis’ ‘total'

(latitude) Year o/e model model model

Other yearsDarwin, N.T.* 1 9 8 4 8 5 o 14 Dec 13 Feb 13 Feb(~ 12ºS) eT2 6 Jan 24 Mar 22 Mar

eA 29 Dec 18 Mar 14 MarDarwin, N.T.* 1985-86 o 23 Dec 20 Feb 20 Feb(~ 12ºS) eT2 6 Jan 24 Mar 22 Mar

eA 29 Dec 19 Mar 14 MarBlacksoil Ck, Qld 1986-87 o 31 Dec 12 Mar 12 Mar(~ 19ºS) eT2 10 Jan 21 Mar 31 Mar

eA 13 Jan 31 Mar 1 AprTufTCrater, N.Z.? 1 9 8 0 - 8 1 o 8 Apr 28 Jan 28 Jan(w 370s) eT2 14 May 25 Dee 6 Feb

eA 18 Apr 13 Dee 16 Jan

Other regionsD u r b a n , R.S.A.1 1978-79 o 17 Jan 11 Apr 11 Apr(w 300s) eT2 8 Feb 21 Apr 25 May

eA 18 Feb 30 Apr 10 JunD u r b a n , R.S.A.3 1979-80 o 16 Jan 23 Apr 23 Apr(~30%) eT2 8 Feb 21 Apr 25 May

eA 18 Feb 30 Apr 10 Jun

* Woodroffe et al. (1988).-f Woodroffe (1982).f Steinke & Charles (1984).

multimodality in annual patterns, including early summer and winter peaks. Thissuggested that other factors were important.

One such factor was rainfall and general moisture because of a co-ordination of leafdevelopment peaks and drier periods (compare Figs 3 and 7). There were consistentlatitudinal trends for sites in very different moisture conditions: first, those sites (sites 14and 15) where moisture was apparently limited during the entire year; secondly, other sites(sites 18 and 23) where it was not limited during any month. However, by contrast,relative peak heights of summer and winter leaf development were apparently influencedby moisture conditions because all tropical sites with maximal peaks during early summer(around October) also had between nine and twelve months of high evaporation each year(compare Figs 3 and 7). There was a progressive increase in putative temperature optimain these sites from the more stable pattern (c. 20 C) observed in temperate sites. Theseobservations suggested that leaf development was controlled by a combination of atemperature optimum and moisture conditions, but field studies of seasonal shoot growthindicated that co-ordination with the reproductive cycle was also important.

Co-ordination of leaf development and reproductive cycles

Two leaf growth patterns were observed during field studies at Blacksoil Creek, onebeing directly related to reproductive development. Appearance of new leaves wastherefore associated with either: (i) terminal and sub-terminal growth of inflorescences(immediately following initiation) during September-October (early summer); or (ii) new

Tropic oiCancer

20

Latitude

North 10

Lat i tude ‘0

South

20Tropic ofCapricorr

30

40

N. C. DU K E

J J A S O N D J F M A M J J A S O N D J F M A M J

J J A S O N D J F M A M J J A S O N D J F M A M J

Months

FIG. ICI. Phenology of Au&n& murinu is depicted in tbj: graphical model over two years and itsfull latitudinal range. It traces periods of peak activity for major phenological events includingleaf fall, putative initiation of the reproductive cycle (notably long days, see text), flowering andfruit maturation. Leaf production phenology may also be deduced, because new leaves generallyappear on trees one month before leaf fall (note Fig. 6, and text). Timing of all these events maydiffer by one or two months at specified latitudes if climatic conditions in a particular site do notcorrespond with overall patterns in Australasia (note, the importance of air temperature andrainfall discussed in the text). Shaded areas show predominant periods when trees carryreproductive parts (note, there is uncertainty about events near the equator and the transitionbetween hemispheres). Circled letters relate to different sections of leaf-fall traces, apparentlydivided in response to reproductive activity; thus leaf fall ‘a’ occurs between one season’s fruitmaturation and initiation of the next, leaf fall ‘b’ occurs between initiation and flowering withinone season, and leaf fall ‘c’ occurs between flowering and fruit maturation, also within one season.

Dotted leaf-fall traces identify predominant trends in variable leaf fall maxima.

131

axillary (and independent) vegetative growth during February-March. These patternswere reflected in concurrent litter-fall collections as either co-ordinate peaks of earlyreproductive material and new leaves, or leaves only.

Extrapolation to the Australasian study revealed considerable variation in respectivepeak heights and occurrence (Figs 4 and 7). In temperate sites there appeared to be only

132 Phenology of Avicennia marina

inflorescence leaves, while in tropical sites the situation varied from the temperate patternto multimodality. In these sites inflorescence leaves were dominant where evaporationwas high for most of the year (9-12 months; sites 10 and 13-16). This may indicate that theplants depend on this behaviour to conserve resources in sites with lower temperaturesand lower moisture conditions. Thus, independent leaf development was possibly anindication of more amiable environments for growth and development of this species. Inthese ‘wet’ tropical sites late summer and winter peaks in leaf appearance (Fig. 7) occurredeither between flowering and fruiting (sites 6, 9 and 12), or just after fruiting (includingsites 1-5). This pattern displayed apparent indirect links between cycles which reflectadditional aspects of resource partitioning. A further indication of this was suggested insouthern temperate sites where changes in the shape of leaf development peakscorresponded to the progressive overlap with fruit maturation.

These phenological trends, plotted with respect to latitude and time, are presented inFig. 10 as a graphical model encompassing at least one complete cycle of reproductivedevelopment over the entire latitudinal range of the species (Moldenke 1960, 1967, 1975;Chapman 1970; Tomlinson 1986). Extrapolation into the northern hemisphere is basedon putative initiation date of the reproductive cycle when daylength exceeds twelvehours, and the observation that events were six months out of phase at comparablelatitudes (e.g. Wium-Andersen & Christensen 1978). In summary, patterns in pheno-events are repeated annually, and their timing and order reflect the latitude at specificsites. Furthermore, reproductive development in higher latitude sites is longer, inresponse to cooler temperatures, and shows considerable overlap between successiveyears. By contrast, phases in equatorial sites (< 9O latitude) do not overlap, although it islikely that more rapid development and repetition of the initiation stimuli, may allowduplication of reproductive events within a single year. Sites between 9” and 17’ latitudetend to have a simple order of events each year, although leaf fall (and leaf appearance amonth earlier) is often bimodal with peaks in winter months and early summer (noted insouthern latitudes as, solid trace ‘a’ for June-August, and dotted trace ‘b’ for September-October, in Fig. 10). The latter, but not necessarily smaller, leaf-fall peak correspondswith the start of the reproductive cycle, itself continuing through the summer months(September-March in southern latitudes). In latitudes around 18’ S, dates of maximalleaf fall are quite variable (Fig. 7), indicating a possible transition to patterns observed inhigher latitude sites with overlapping pre-anthesis and ‘leafing’ phases. Sites between 19’ Sand 32’ S show a single leaf fall maxima (solid trace ‘b’ in Fig. 10) following putativeinitiation. Reproductive development in these sites occurs over most of the year, with pre-anthesis development over summer and post-anthesis development during early winter.In latitudes greater than 32’ S, phenoevents, notably fruiting and ‘leafing’, convergeduring warmer, summer months (Figs 7 and 10). In such sites, phenoevents are noticablyabsent during winter months, although trees carry reproductive material all year round,and fruit maturation occurs within two or three months of next year’s flowering.

It is clear that A. rnurinu is an extraordinarily adaptable plant and the wide latitudinalrange of this mangrove apparently exists because of its flexible growth patterns.Nevertheless, this range appears to be limited chiefly by reduced fecundity in colderclimates. For example, in higher latitudes (5 35’s) and for lower mean dailytemperatures (< 18 C), flowering success approached zero (Fig. 9). Therefore, a slowingof developmental rates and the overlap of leaf growth and reproductive events, coupledwith an ultimate intolerance to winter chilling at -3 ‘C (Wardle 1985), presumablycombine to limit the natural latitudinal extent of A. murim2 within otherwise suitablehabitats.

N. C. DU K E 133

.

ACKNOWLEDGMENTS

Facilities and assistance for this study were provided by both the James Cook Universityand the Australasian Institute of Marine Science. The Australasian litter-fall study wasinitiated by J. S. Bunt in 1982 and involved the assistance of more than twenty volunteers(Table 1). The study in the Murray River was assisted by members of the ANZSESCardwell Range Expedition of 1986-87. Thanks are due to all these people, to E. Drewwho developed the program to calculate irradiance and daylength, and to B. Jackes, K.Boto, J. Benzie, A. Robertson and J. Wu Won for advice, discussion and assistance.

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(Received 29 September 1988: revision received 17 June 1989)