,i, rlil,( \ltu THE ROLE OF BIRDS IN THE REPRODUCTION OF ÀN ÀRID ZONE
POPULÀTION OF GREY I.{ISTLETOE MYEHÀ OUANDANG
( LORANTHÀCEÀE )
Nick Reid
Department of Botany, University of Àdelaide
Thesis s'¡bmitted for the degree of Doctor of Philosophy
December 1984
FRONTISPIECE: Àmvgmg quardanq parasitic on çrestern myall Acacia DaDvroceEBg at Port Àr.rgustã, Souttl H¡stralia. The mistletoe canopy eras supported by numerous hÃustorial branches growing from the two main limbs of the host.
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q0NIENrs
ÀBSTRACT DECLÀRATION ÀCKNOWLEDGEMENTS t. THE PRoJECI Page
1.1 INTRODUCTION 7
7.2 LITERATI.JRE - THE BIOLOGY OF MISTLETOES 2 1.27 Biogeogrraphy and systematics 3 1.22 The mistletoe haustorium 4 1.23 Ecophysiology 4 7.24 Host specificity 5 7,25 Host mimicry 6 7.26 Àustralian mistletoes and European settlement 6
1.3 EMBRYOLOGY ÀND POLLINATION BIOLOGY IN THE LORANTHÀCEÀE 7
7.4 SEED DISPERSÀL OF MISTLETOES 7.41 À world survey 10 1.42 Mistletoe dispersal in Australia t4
1.5 THE HISTLETOEBIRD 15
t.6 THE SPINY-CHEEKED HONEYEATER 18
t.7 ÀRID ZONE ''UNPREDICTÀBILITY'' AND LIFE HISTORY ATTRIBUTES 79
1.8 RESEARCH ÀIMS 2t
2. STUDY ÀREÀ
2.1, INTRODUCTION 26
')) MIDDLEBÀCK STÀTION 26
2.3 CLIMATE 2.31 General 27 2.32 Rainfall during the study period 28
2.4 TOPOGRÀPHY AND SOILS 29
2.5 VEGETATiON 29 2.57 Chenopod 1ow open-shrubland 30 2.52 Western myall low open-woodland 30 2.53 B1ack oak loç¡ woodland 31
2.6 BI0LOGY 0F IIIESTERN MYÀLL 31 3 HOSTS_ÀND-POPULÀT I ON STRUETURE-OF-ÀUIEUÀ OUANDANG
3 1 HOSTS, DISPERSION ÀND ÀGE STRUCTURE 3 71 Introduction 38 3 72 l.lethods 39 3 .13 Results 3 .131 General observations 40 3 .732 Host specificity of mistletoes in the trapping area 47 3 . 133 Àmveme ggendang: age indices 4t 3 .134 Ànyeng suandanq infection of western myall 42 3 .14 Discussion 3 .747 The abundance of Àmvema q¡sndanq 43 3 .142 Host specificity 44 3 . 143 Haustorial structure 45 3 .744 Àge structure of Amvema guandanq 47 3 .145 Patterns of western myall infection 48
3 2 DEÀTH ÀND DEBILITY 3 2t Introduction 50 3 22 Sampl ing considerations 50 3 23 Methods 51 3 24 Results 3 .247 Amyeme quenda¡g 52 3 .242 lygiana exoqalpi 53 3 .25 Díscussion 53
4 REPRopUCTIVE PHENoLoGY 0F AMYEHÀ_QUÀNDÀNG
4 .7 INTRODUCTION 68
4.? METHODS 4.27 Ì,feasurement of flower and fruit abundance in mistletoes 69 4.2? Floweríng and fruiting in other perennial species 77
4 .3 RESULTS 4 .31 Amvemg suandanq reproductive phenology 4 . 311 Bud initiation 72 4 .312 Flowering season and flower production 72 4 'r4 a Fruiting seasons and fruit production 74 4 . 314 Relationships between individual flower and fruit production 78 4 .32 Flowering and fruiting ín Lvsiqng exocarr¡i 78 4 .33 Flowering and fruiting of other perennial species 79
4.4 DISCUSSION 4.41 Individual patterns of reproduction in Àmveme quandeDg 80 4.42 Patterns of flower and fruit a-bundance in Àmvema quandang: implications for polIÍnation and seed dispersal 82 4.43 Seasonality in flowering and fruiting 83 4 .44 Effects of drought on reproductive phenology 84 5 THE ECOLOGY OF THE SPINY-CHEEKED HONEYEÀTER ÀND },ÍISTLETOEBIRD
5.1 INTRODUCTION
5.2 },fETHODS 5.21 Birds eating mistletoe fruit 108 5.22 Bird census 108 5.23 Spiny-cheeked honeyeater and mistletoebird diets 109 5.24 Territoriality and behaviour 717
5 3 RESULTS 5 31 Birds eating mistletoe fruit tt7 5 .32 The spiny-cheeked honeyeater 5 .321 Diet tt2 5 .322 Faeces tt4 5 .323 PopuJ.ation dynamics 115 5 .324 Breeding 716 5 .325 Pair bond tt6 5 .326 Site fidelity and territoriality 7t7 5 .33 The mistletoebird 5 .331 Diet tt9 5 ,332 Faeces t27 5 .333 Population dynamics 122 5 .334 Breeding 723 5 .335 Site fidelity 123 5 .336 Behaviour 124
5.4 DISCUSSION 5. 41 Birds and mistletoe fruit t25 5.42 Comparison of foraging observatÍons and time budgets to elucidate diet 727 5 .43 spiny-cheeked honeyeater 5 . 431 Diet t28 5 .432 Population dynamÍcs 131 5 .433 Territoriality t3t 5 .434 Breeding 133 5 .44 Mistletoebird 5 .447 Diet 135 5 .442 Influence of diet on Iife history 136
6 BREEDING SYSTE},Í AND POLLINÀTION ECOLOGY OF ÀMYEMÀ OUÀNDÀNG
6 .7 BREEDING SYSTEH ÀND POLLINATORS 6 .7t Introduction 764 6 .72 Methods 6 ,727 Timing of anthesis and floral lifespan 165 6 .122 Breeding system 165 6 ,723 Experiments measuring seed set t67 6 ,724 Nectar production 167 6 .I25 Pollinators 168 6 .13 Results 6 .131 Floral phase 769 6 .732 Breeding system 770 6 .133 Experiments measuring seed set from hand pollinations 172 6 .134 Nectar production 773 6.135 Pol.I inators Diurnal flying insects 773 Ànts 174 Hoths 775 Birds 175 6.74 Discussion 6.147 Floral phase 176 6.142 Breeding system 778 6.143 Experiments measuring seed set t79 6.744 PoI I inators 181
6 .2 POLLINATOR EXCLUSION EXPERI},fENTS 6 .21 Introduction 183 6 22 Methods 183 6 .23 Results 185 6 24 Discussion 188
7 FRUITING DISPLAY, INEECTION RENIBEMENTS. ÀND SEED_DISPE8gÀL
7 .t FRUITING DISPLAY 7 .71 Introduction 274 7 .t2 Methods 275 7 .13 Results 7 131 The ripe fruit 215 7 732 Ripe fruit production and removal 276 7 133 Seed predation 2t8 7 74 Discussion 2t9
7 .2 GERMTNATION ÀND HYPOCOTYL GROWTH 7 .27 Introduction 227 7 .22 Methods 221 7 .23 Results 222 7 .24 Discussion 224
7 .3 INFECTION ÀND ESTÀBLISHMENT OF ÀHYEMÀ QUÀNDÀNG SEEDLINGS 7 .31 Introduction 227 7 .32 Hethods 227 7 .33 Results 228 7 .34 Discussion 237
7 .4 SEED DISPERSÀL BY THE SPINY-CHEEKED HONEYEATER AND UISTLETOEBIRD 7 .41 Introduction 235 7 .42 Methods 7 .421 Seed vector efficiency 236 7 .422 Seed vector effectiveness 236 7 .43 Results 7 .431 Seed vector efficiency Histletoebird 237 Spiny-cheeked honeyeater 239 Comparison of the seed shadows of the mistletoebird and spiny-cheeked honeyeater 240 7.432 Seed vector effectiveness 240 7 .44 Discussion 7.441 Seed vector efficiency 241 7 .442 Seed vector effectÍveness 243 I CONCLUDING DISCUSSION
I 1 HUTUÀLISÌ.Í BETIüEEN ÀUYEHÀ QUÀNDÀÌ,¡q, ÀND THE SPINY-CHEEKED HONEYEÀTER AND MISTLETOEBIRD 270
8.2 THE EVOLUTION OF SPECIÀLISED MISTLETOE-FEEDING FRUGIVORES 278
8.3 HOSTS ÀND HÀBITÀT STÀBILITY 279
8.4 BIOLOGICAL PROCESSES AND ARID ENVIRONMENTS 289
APPENDIX 1 - Analysis of mistletoe distribution across hosts 282
APPENDIX 2 - The bírd community 285
ÀPPENDIX 3 - Analyses of variance: origina] data and tables 289
ÀPPENDIX 4 - Manuscript of Reid (1985) 302
REFERENCES 347
PLÀTES THESIS AMENDMENTS, MARCH 1985
During examination of the thesis, one examiner made the comments and queries which are reproduced beIow. In response, I have amended the text in several places and have appended a list of notes to explain or clarify certain points. The notes are cross-referenced to the appropriate text. I have also appended 'Conclusions' sections for Chapters 3-7 to aid interpretation of the main themes of the ç¡ork. The concluding statements ought to be read at the end of the relevant chapters of the thesis.
EXAMINER'S CRITIQUE
Chapters 1-3 - no special remarks.
Chapter 4 p. 77 Eop, tll. 'tfhat is this X2 testing? !{hat association? ' Make expliciÈ Èhe qrestion that is answered by examinatiôn of spatial gattern of pfãG possessing sinilar reproductive phenology -(e.9. 5r. 78 top, P' 74 botto¡n)' p. 80, f3, I 5ff. Conclusion is unwarranted. How much selection exists for outcrossing has not been esÈablished. p. 91, f . re correlation,.of flower number with canoPy size. l'lhere are the data? Also: "...stable þatterns...will change... " is a confusing statement.. Table 4.5. It is not clear to me whaÈ this Èab1e says - eiÈher what the data represent or whaÈ theY nean.
P. 85. 9¡hy not sum. fruit and pedicels to geE toÈals? p. 79 and p. 86 top. Lysiana: are Èhe yearly differences significant? Should do stats on Amyema vs f.ysiana to documenÈ this assertion.
Discussion does noÈ seem Èo cover aims of study as lafd out on P' 69¡ especially *1 and *3.
Chapter 5 g. L22-3. wtry no regressions of nistletoe bird abundance vs tfme, as done for honeyeater?
P. I31, tl3. But che regressions on p. 115-6 showed no relationship of fl./ft. abundances and bird abundances, so the conclusion seems arguable. !'Ihy not, have a sumnary staÈ,ement at the end of chapÈer ÈhaÈ relates result,s to quesÈions on p. 107?
What is the interpretation of the findings Èhat the birds de-oend so heavily on Amyema' yet neither abundance nor activity is related to abundance of this resource?
Chapter 6 P. 164, fI. the prediction should not include the ¡nssíbiliÈy of sfunilarity. "lúc change" is not a tesÈ of hypothesi-s. P. 168. The frequency of bird visits was recorded on only 2 days. This d,oes not seen at all adequate, given how much seasonal variation there seems to be in other ecological aspecÈs of this system. P. 174 and Table 6.11. Ogyris is said, in Tab1e, Èo be a frequent vÍsiÈor; which seems to contradict text. Table and Text also do not quite agree re colletids. p. 178, top 2 lines. On what data is this statement based? p. 180, 12. Low set lrom hand pollination could also be from red.uced viability of stored, pollen. p. 182. If birds visiÈ ð phase flowers preferenÈially, and this gattern of necÈar production increases pollen removal, then whaÈ effect does it have on pollen delivery? I.lhy do birds visi'. T phase flowers? Is pollen viable for nany hr? Maybe bees are better pollinators than you think. p. 184. Mistletoe bird drogpings inside cage: Could the birds be ¡rerching on Èop of cage? P. 185. floral Èurnover. This value could apparently be negative, if numbers of fl. and buds increases. Yet you ignore low values (bottom of page) for some calculations. Is this a good idea? p. I89, .|13. Intermittent bagging also reduces frequency of pollinator visits. Therefore, lnây not be merely a "bag effect." Needs a su¡nmary, as do other chapters. What is the take-home message, in brief?
Chapter 7
p. 2L4. Competition hypothesis (reI. to sÈaggered Èiming) is much Ín question. See e.g. l.¡aser 1982 in Handbook of Experimental PollinaÈion Biology, and look for papers by B. J. Rathcke on phenology in particular. liso 61."s",- r'l 9i Otrc'''ft6t': ft : ),ìt-í'. fig. 7.2. Why use different values (t, #f) Ín Èhese graphs - should all. be sa¡ne Y-axis. g. 22O, fl, too. But there were large differences in Èime required for ripening, so more than sinple order is involved. p. 227. Purpose of using dead twigs is not clear; how could you expecE the seedlings to survive very lonq? p. 232 top. But what íf seed landed in a fissure? Chapter I p. 273-4. But, is the "monoculture" of grey mistletoe the case in all Íts range, or just where you studied iÈ?
p. 275, fI. #3 doesn't seem Èo have much to do with Àmyema, though. NOTES OF CLARIFICATION
1. p. 77. The X2 test evaluated the null hypothesis that temporary suspension of fruiting in a season was distributed among individuals independently of continuous fruiting across two or more seasons. 2. The finding that plants which had similar individual flowering (p. 74) and fruiting (p.77) phenologies were not clustered in groups along the traverse to the spatial exclusion of other such groups has two important corollaries. First, an appropriately sized sample of plants in one place ought to encompass the major phenological variation encountered throughout south-western Overland paddock. secondly, processes centred on Amygme queldeng phenology which are studied in one site may be assumed to occur in adjacent areas, because significant temporal differences in interactions between plants and theír mutualists and predators are unlikely to occur betu¡een sites. 3. p. 81. Since much of the individual varÍation in flowering phenology appeared to be related to the vegetative size of mistletoes and not genetic differences, the relative phenological performance of individuals would be expected to change in time as individuals increased in size or senesced. No data were collected on individual canopy sizes. 4. p. 85. Basal epicarp halves were not counted (they were rated to the nearest order of magnitude, p. 70). Therefore I was unable to sum fruits and epicarp halves to counter the problem of variable fruit removal by birds. 5. p.79. The number of individual Lvslang gxcqarpi which annually flowered and fruited declined significantly between 1981-83, as indicat.ed in the following tables. The X2 tests evaluated the null hypotheses that the proportion of traverse plants which (a) flowered and (b) bore ripe fruit in each year were equal.
(a) Me¿imum !UBþeE of plants_wilh llowggg Year 7987 7982 1 983
0bserved 70 62 42
Expected 57.55 56.75 60.7s
Xt = 8,97x, 2 d-f.-
(b) MaXj4um_¡umbgr ¡f plenlS_s¡rth_$pe_frUf!
Year 1981 7982 1983
0bserved 54 56 15
Expected 39.61 43.62 42.48
E = 26.52***, 2 d_L 6. p. 83. The prediction of the arid zone unpredictability hypothesis that arid zone perennials ought to have aseasonal reproductÍve cycles in order to capital.ize on effective rainfall whenever it falls is not supported by these data.
7. p. 137. Mistletoebird abundance may be a function of Àrnyema qugda¡g ripe fruit production less the quantity taken by spiny-cheeked honeyeaters, or perhaps even of arthropod availabitity. Alternatively, food abundance may not lÍmit místletoebird numbers. For instance, if most birds are transitory in the area, the population size at Middleback may represent a dynamic and variable equÍlibrium state largely dependent on extrinsic rather than intrinsic factors in the system. Further data are required to test these hypotheses.
8. p. 131. Although the regression analysis (Table 5.10) demonstrated that ÀnygUg zuendang flower abundance accounted for a significant degree of the variation in spiny-cheeked honeyeater numbers, the non-signifÍcance of the partial regression coefficients for the other plant variables does not imply that such variables have no predictive power or are unimportant influences on honeyeater density. l{ithin the constraints of Lhe data-set available, the analysis failed to attribute the variables with any explanatory pou¡er over and above that of A. quanda¡g flowers. Further analysis of the data is warranted, without the use of A- ggandqng flowers, to ascertain whether the remaining dependent variables are useful predictors. 9. p. 774 e Table 6.t7. The column in Table 6.11 entitled'Frequency of Visitation to Amye¡e zue¡deg Canopies' records the frequency with which animals were seen about mistletoe canopies, not the relative frequency with which they behaved as effective pollinators of A* zuendang flowers. Thus Qqvqig qma¡yllig Eegldignalis was frequently observed flying around mistletoes but infrequently visited flowers for nectar. Similarly, the small colletid Legfeqfqssg¡ (Caffomelille) bees, although frequent visitors to mistletoe canopies and flowers, r.,ere comparatively ineffective pollinators, as explained in the text. 10. p. 178. There are no widespread or abundant plant species with bird flowers which overlap in flowering season with Ànyemg epeldanq in the western myall woodlands of north-eastern Eyre Peninsula.
11. p. 185. Flowering in Àmyema E¡gnda¡g was determinate. Buds were initiated late in each year and grrew slowly across the summer to begin flowering in autumn (Chapter 4). Flower turnover sras never negative, because the number of buds and flowers did not increase on branches after bud initiation. The variation in seed set ratios based on flower turnovers less than 20 was congiderable in comparison to data based on }arger turnovers of flowers. Àccordingly, ratios based on flower turnovers less than 20 were igrnored. 72, p, 227. EsLablishment of stem-parasitic mistletoe seedlings, !-g^ the transition from the free-Iiving phase (u¡hen the plant is dependent on nutrient reserves in the endosperm) to the parasitic phase (when it becomes dependent on the host for water and mineral nutrients), is difficult to define (Liddy 1983). Accordingly, I adopted the criterion that seedlings established on living host stems if they survived longer than the maximum longevity of seedlings in the free-Iiving phase deployed on dead sticks. 13. p. 232. SeedlÍngs which attempted to penetrate fÍssured bark did not establish. The fissures on smaller stems were too small to admit the whole holdfast r¿hich requires a flat surface to develop and subsequently penetrate the host periderm. Fissures in the bark of larger stems were too rough and fibrous to permit effective holdfast development.
14. p. 275. SmaII ants lridomyr¡ex sp. (gp F) occurred in hiqh density on some Amvema gqgndanq p).ants in summer on account of eurymelid and scale insects, and the ants took nectar at flowers on çrarm days throughout the flowering season. If A- guandgDçl flowered in summer rather than winter, the density and aggression of small ants might increase to levels observed on summer flowering tysians e¡gqqrB¡.
CHÀPTER CONCLUSIONS
3.5 CONCLUSIONS The large canopies of f,rnyema qqgldenq parasitic on western myalls are a conspicuous element of the landscape in the !'lhyalla region. The mistletoe population is effectively host specific to myalI. The abundance of the mistletoe is not a consequence of the ecological disturbances accompanying european settlement, but a natural feature of the population biology of A- ggenda¡g in the region. The density of AUyene guandang averaged 189 haa and 6 myalla in the trapping area. However, the population was distributed contagiously, with a large proportion of individuals parasitisÍng a small number of host trees with large canopies. Most mistletoes çrere young, as judged by their non-reproductive status, few haustorial branches, and the thinness of the host stems on which they grew. The population thus appeared to be reproducing and maintaining itself . The haustorium of Amyema ggandang was characterised by extensive Iateral development of endophytic strands in the host phloem on either side of the primary connection. The cortical strands gave rise to secondary haustoria in the host wood, producing aerial shoot systems at points along the infected portion of host branch. This mode of vegetative spread enabled individuals to persist as secondary modules long after the primary connection had broken down. Two lines of evidence suggest that the oldest mistletoes may reach a considerable age, certainly older than 30 yr. First, onLy 4% of a sample of large individuals died in a monítoring period of 3 yr which included a period of severe drought. Second, since A- quandanq could only establish on the thinnest stems, individuals with massive haustoria ramifying through the Iimbs of old western myalls had conceivably persisted with their hosts for most of the life of the trees. The severe drought had a debilitating effecl on 20% of the mistletoes monitored. One or more major haustorial branches died, leading to reductions in canopy volume. Very few individuals died, however, owing to the persistence of the younger secondary modules. tyggne exocarpi was also widespread in the lthyalla region, parasitising most species of tree and tall shrub, as well as Àmyemg ganda¡g. However, it rarely occurred on ç¡estern myalls. L gXqqggp! only constituted tt"z. of the mistletoes in the trapping area where its most frequent hosts were f,- qge¡denq and !¿ocarpqg aphyllus. During the 29 mo monitoring period, siginificantly more individuals of L^ exocarÐi died on À- ruandalg hosts, due to the death of a major haustorial branch of the host, than on non-Amyemg hosts.
4.5 CONCLUSIONS Àmvgme quq¡dang displayed a regrular annual cycle of reproduction. Peak flowering among individuals was synchronised and generally occurred in mid winter. Most individuals produced rÍpe fruit most of the time, and a few fruited continuously. In consequence, ripe fruit was available year-round aLbeit in varying abundance. The largest standing crops occurretl in sumrner. There was considerable variation between individuals in the date of the onset of flowering, the length of the fJ.owering season, and the length of the fruiting season. The variatÍon was correlated with the reproductive ouput of individuals which, in turn, appeared to be J.argely a function of canopy size. Thus, much of the variation between individuals in reproductive performance çras non-heritable. Nevertheless, the differences between individuals were consistent in consecutive years, underlining the degree of predictability in the reproductive patterns of both individuals and õf the population as a whole, at least in the short-term. Severe drought did not lead to a failure in either flowering or fruiting in !¡yema qugn{gng, it merely retarded the development of br.rds and the maturation of fruit, resulting in a Low standing crop of ripe fruit in a dry summer and a 4 mo delay in the onset of flowering in the following winter, well after the drought had broken. The ability of A- quandang to maintain flower and ripe fruit production in drought reflected more than the advantage that parasitic mistletoes receive in utilising the relatively permanent transpiration stream of the host under conditions of low soil moisture, because lvsia¡a exocarp! reproductive output dectined in successive years as a result of the drought. The reproductive cycles of seven of eight perennials studied displayed marked seasonalÍty, although some appeared more flexible than others r¡ithin seasonal constraÍnts. Seasonality in plant reproductive behaviour is inconsistent with the expectatj.ons of the arid zone unpredictabi I ity hypothesis.
5.5 CONCLUSIONS The spiny-cheeked honeyeater and mistletoebird r¡ere the only important consumers of Amyeme zue¡dg¡q fruit at Middleback. The reproductive phenology ot- Ànyeng rya¡dang was central to the ecology of the spiny-cheeked honeyeater. Individual birds u¡ere generally faÍthful to terrÍtories of two to several hectares in myall woodland which contained large numbers of mistletoes. Territories erere held in pairs and some birds ü,ere paired with the same mate for the duration of the study. In the flowering season of Àmyeme quandang, spiny-cheeked honeyeaters spent most of their foraging time feeding on nectar in order to meet their carbohydrate reguirement. Outside the flowering season, birds turned to the fruÍts of 4- quandEnq. The large numbers of seeds consumed per day probably met most or aLl of their carbohydrate requirements. Birds also foraged for insects and the nectar and fruit of other food plants in their territories. Higher population densities $rere sustained by flowering in winter than by fruiting in summer. Nevertheless, even in severe summer drought, birds returned to their territories at intervals and searched them for mistletoe fruit, as welI as foraging further afield. The mistletoebird was also dependent on Àmyema gganQanq for food in the study area. Birds were present all year-round, and subsisted on a diet of mistletoe seeds which met their carbohydrate requirement. Mistletoebirds occurred ín low density, their abundance fluctuating Iittle between the seasons, although a significant long-term decline in counts coincided r.¡ith the drought. Fluctuations in abundance were not related to changes in the abundance of the standing crop of ripe fruit. Some individuals iesided in the area for up to 1 yr but most birds were transient, only staying for a few days or weeks.
6.3 CONCLUSIONS The Ì,liddleback population of Amygme qugndalq $ras facultatively outcrossing. Fì.owers $rere equally receptive to cross- and self-pol).en on the basis of pollen tube penetration of the stigma and stylar tissues, and no significant difEerence was detected in seed set after controlled hand pollinations with self- and cross-pollen. In these respects the breeding system wa.s similar to a temperate Victorian population of the same species. However, unlike thal-. popr.rlaLton, autogamy was poterrtially important in seed seL and the flowers were protandrous. Pollen was dispersed largely within the firsb 24 hr of floral life when stigmas were unreceptive, whereas most 2-10 d oLd flowers çrere receptive to poJ.Ien. The breeding system therefore tended towarcls outcrossing in cr:m¡:arison to the Victorian population, which is incrrnsisterrt wiLh expectations of the arid zone unpredictability hypothesis. The Iikely selection pressures which have led to this degree of outbreecling are a greater degree of pollinaturr fidelity and efficiency at Middleback, a greater abundance of safe sites for seeds and the relatively stable habitat offered by western myall limbs and branches for mistletoes. Flowers were visited by a l¡road spectrum of animals for nectar or poì"len, including many species of bees, ants, moths and birds, as well as wasps, butterflies ancl fIies. The most effective pollinators were thought to be s¡riny-cheeked honeyeaters, and to a lesser extent, singing honeyeaters and a specÍes of megachilid bee (orrly active in spring). The hypolhesis of Forcl el al- (1979) that Amygma fLowers are pollinated mainì.y by birds but that insects may pollinate flowers in the absence of birds was experimentally supported. I showed that (1) seed set was maximal on branches exposed to all pollinators including honeyeaters; (2) an appreciable number of flowers exposed t-o insects br.:t not birds set frlrit; and (3) relative to controls, seed set on branches accessj.ble to insects but not honeyeaters r.Jas lower in winter when insects were least active than in ar.¡tumn or spring. The data in (3) meant that insects must have fertilized more flowers inside cages in autumn and spring t-han in winter, since seed set in autogamy treatment-s riid not shot¡ a similar pattern to that inside cages, nor coul.d the results be explninerl by herbivore grazing.
7,5 CONCLUSIONS The annual pattern in ripe fruit production of Amyema ggançlang Lras variable, most fruit ripening early in the fruiting season in summer. Procluction declined to low levels across the winter flowering season. This pattern was correlated with the consumption pressure exerted by frugivores. Spiny-cheeked honeyeaters ate much fruit in summer, whereas in winter the small population of mistletoebirds constituted the sole consumers. Although developing frrrit persisted on plants for long perÍods, seed predation was negligible, probably due to thÍck epicarp of young fruits and the cryptic coLonr of both irnmature and ripe fruits. Àßyema qgêndanq seeds germinated in all seasons, and seeds defaecated by spiny-cheeked honeyeaters and mistletoebirds generally showed no difference in survival or growth. InfectÍon was most frequent on the smooth grey stems of western myall, which were 3-6 mm in diameter. E-qtablishment success declÍned on increasingly thicker and more fissured stems, ancl no seeds infected stems greater than 16 mm in diameter. Herbivorous insects accor.¡nted for the loss of 15-35% of seedlings deployed on living myall stems throughout the year, but the predation rate did not vary seasonally. Seedling death at various stages of the free-living phase, including germination failure, misdirected hypocotyl growth and seedling mortality in the holdfast phase, rras more frequent, in summer than winter. The seeds of Àrnyemg ggq¡dang require a biotic vector to release them from the epicarp. The general features of the seed shadow of the spiny-cheeked honeyeater and mistletoebird differed dramatically. Most seeds dispersed by spiny-cheeks fell on to substrates, particularly thin shoots or large branches in tree canopies. HistletoebÍrds dispersed most seeds to intermediate sized branches by depositing defaecated seeds on the perch. However, the probability that a seed was dispersed to a thin living myall branch less than 6 mm in diameter was similar for each species, of the order ÀÞ_9TBÀET
Àmyema qug¡da¡g is an abundant, host-specific parasite of western myaJ.I lcacia pep[fqcåfBe in the Ílhyalla region of arid South Àustralia. Àn extraordinarily specific mutualism exists between Amvema gUEndang, and the spiny-cheeked honeyeater Àçanthaqenvs rufogqlarig and mistletoebird DlcaeUg hirundinaceu!!. The birds receive a pennanent carbohydrate resource in fruits or nectar, and the plant maintains permanent populations of dispersers (mistletoebird) or pollinators-cunr-dispersers (spiny-cheeked honeyeater).
Àmyeme qgandgDq has a regrular annual cycle of reproduction. Peak
flowering was synchronised anong individuals and occurred in mid winter.
The main season for fruit maturation Lras summer, but large indivíduals
produced ripe fruit most of the time and a few fruitect continuously. Most mistletoes persisted with reproductive activity through a severe drought,
although flowering r¿as 4 mo late compared to previous years.
The reproductive phenology of Amyeme gge¡Qanq was central to the
ecology of the local population of spiny-cheeked honeyeaters ÀcanÈhaqenys rufggglggrg. Birds obtained most of their energy requirements from the
floral nectar of the mistletoe in winter and from the fruit in summer. Territories in woodland containing mistletoes were defended by pairs
throughout the year when food was locally sufficient. Higher bird densities were sustained by the flowering of à- ggandcng in winter. Nevertheless, even in severe summer drought, birds returned to their former terrÍtories at intervals and searched for mistletoe fn¡it.
Histletoebirds s,ere present in low density throughout the year, and
subsisted on a diet of Ànygmg gggDdanq fruit and a few insects. Some individuals resided in the area for up to 1 yr, but most were transient, staying for periods of a few days to a few months.
ÀBvems quandanq was self-fertile and facultatively outbreeding, and the flowers were protandrous. Flowers were visited by a large array of nectar- or pollen-harvesting ants, moths, bees, butterflies, wasps and birds. Spiny-cheeked honeyeaters were the most important pollinators. Bird pollination effected the largest seed set, but insect pollination was potentially responsÍble for 20-30% of seed set in autumn and spring.
ÀnygEg quaDdang produced reletively large, cryptically coloured fruit. The spiny-cheeked honeyeater and mistletoebird were the only leqitimate frugivores which consumed fruit in quantity. Both ç¡ere similarly efficient in dispersing seeds to the thinnest stems of western myall, which were most susceptible to infection. A pilot study of mistletoe seedlings in western myall canopies permitted a majority to be classÍfied as to the bird responsible for their dispersal. Most of the established seedlings had been dispersed by spiny-cheeked honeyeaters rather than mistletoebirds.
The key features of the interactions between À- suandanq and its avian associates which differ from most vertebrate-plant mutualisms are: (1) the abundance of the plant in western myall woodland in relation to other nectar producing plants for birdsi (2) the year-round production by À- quandanq of the primary source of fruit or nectar for both birds;
(3) the facultative specialisation of the spíny-cheeked honeyeater and mistletoebird for f quandanq fruit and nectar; and (4) the reluctance or inability of other fnrgivorous birds to consume f qugndang fruít in quantÍty. The reproductive attributes of A$yemg quanda¡g have probably evolved in response to the presence of sedentary large honeyeaters, such as
the spiny-cheeked honeyeater, capable of doubling as pollinators and dispersers. The mistletoebird is only a recent colonist of Àustralia from Indo-Halaysia, arìd has probably had Iittle influence on the evolution of the fruitÍng displays of Àustralian mistletoes. Neither bird specÍes has
obvious adaptations resulting from interactions with ¡- E¡q¡çlanq.
¡rC¡üotJLEDGEÌ{ ENT5
I am irdebted to my supenrisor, Dr Rob Lange, for his gupport, advice ard frierdship dr:ring the str^dy, ard for the opportunity to participate in the Hiddleback progrrarune. I an similarly gratefuJ. to Lesley, Àndrew, Penan and Don Nicolson, who accepted my cardidature for a l'fiddleback degnee, tolerated the research on their sheep stations, ard aided and abetted my sojourns in the bush. David Paton sr:ggested the field of research, readily accepted part of the academic burden of supenrision, ard listened to the guestions of a nervous doctoral student wÍth many half-baked ideas. ¡any people materially aided ny work or spent time discussing it with ne
over a beer. Chief amottsI them were Kym Nicolson, Hark Stafford Smith, Leith
EdingLon, Penny and David Paton, Jackie Reid, Becky and Stan lloodell, Dave ÀIIen
and Àndrew Johnson. BiII Venables showed admirable restraint when guestioned for too long on statistical matters. Judith King, Robert Fisher, Eric Matthews, Terry Houston, John Greenslade, Ted Edwards and Gordon Gross promptly identifÍed insects. Ànthony Fox and Peter Dorsett were more than useful at practical things in Àdelaide. Mark Stafford Smith, David Paton and Bob Lange read, commented on ar¡d edited the first draft of the thesis. BílI Venables, Stan lloodell, HuSh Ford ard Steve Morton criticised parts, and Jane Roberts proof read the final manuscript at short notice. Due to their efforts, the remaining errors are a small fraction of the original.
My wife, Jackie, and my parents, l,luriel and Ross, supported me morally ard financially over a long period. Hy parents provided the eguivalent of thousands of dollars of research funding in vehicle loans, without çhich little could have been accomplished. Jackie tolerated beirg a l'iiddleback widow for much of the time, coped with receding deadlines, and then spent weeks drafting the diagrams, copyir¡g, word-processing and pastirg to see the thing finished. thankyou for being just right.
The work was supported by a Commonwealth Postgraduate Research Àward.
The thesis is dedicated to the long-suffering Bu/lt and O/tl who made it alI worthwhile. -,c'\:
ÇHÀPrER 1
THE PROJECT
7.T INTRODUCTION
The reproduction of stem-parasitic mistletoes and their dispersal by .,1 birds have fascinated people since ancient times (Kuijt 7969: Calder 1983). Most mistletoes have fleshy fruits which are eaten by frugivorous birds. The birds subsequently disperse the seeds by regurgitation or defaecatÍon. The
mutuaLisms between mistletoes and birds also extend to pollination systems,
rnany mistletoes having large colourful flowers exhibÍting a bird pollination
syndrome (Kuijt 196Ð. The evolution of special.ised mistletoe-feeding birds and the possibility of reciprocal dependence between the plants and birds have led to the belief that mistletoes and certain birds are coevol.ved (Calder 1983; Barlow 1983).
Much of our knowledge of the ínteractions between mistletoes and
birds comes from the classic literature (Keeble 1896; Ashworth 1896; Wetmore 7974; Ridley 1930; Desselberger 1931; Ali 7937: Docters van Leeuwen 1954). A number of studies have been reported within the contemporary framework of evolutionary and ecological theory, but most have addressed ornithological aims without considering the Iikely importance of the interactions in the evolution of mistletoe life histories (ciIl & I,lolf 7975: Walsberg 7975, 7977; Liddy 7982a,1983; Godschalk 1983a,b). Two studies have considered the
consequences of bird-plant mutualism for the evolutíon of the mistletoes concerned. Bernhardt (1983b) summarised investigations of the floral biology
of Victorian [pygqa species. He concluded that coevolution with pollinating birds had been diffuse, and emphasized competitive interactions between congeners and the ecological influence of different hosts as the main evolutionary determinants of misttetoe floral displays. 0n the other hand, Davidar's (1983a) description of the dependence of a guild of Indian Page 2 mistletoes on a flowerpecker Dicagum concolor for both pollination ard seed dispersal is suggestive of a more specific pattern of adaptation in the mistletoe f]ora.
This study examines the ecology of the mistletoe, À¡nyemg quandanq (Loranthaceae), and two bird species, the spiny-cheeked honeyeater
Acanthaqenys rufoqularis (Meliphagidae) and mistletoebird Dicaeu$ hitrr4dllegeg (Dicaeidae), with the aim of determining whether the life history attributes of both plant and birds are an evolutionary outcome of their mutualism. Fieldwork was conducted in arid woodland in the lthyalla region of South Australia. The study site was chosen primarily for pragmatic reasons. The University of Àdelaide's Botany Department, has a research facility, the Middleback Field Centre for Àrid Zone Studies, on a pastoral Iease near t'lhyatla. Mistletoes are abundant in the region, and the wooded formations of the area are Iow in stature. Therefore, all mistletoes and their habitat (tree canopies) were readily accessible. À revÍew of literature is provided in the following sections. The review is selective, providÍng detail in those areas of the biology of mistletoes, their attendant bird species and the reproduction of arid zone perennials, of relevance to the work reported in subsequent chapters. À plan of the thesís is shown in Figure 1.1.
7,2 LITERATTNE - THE BIOLOGY OF MISTLETOES Almost all mistletoes are aerial stem parasites. Às a group, they have been extensively studied in the United States and elseç¡here because of their economic importance (Hawksworth 1983). However, studies of Àustralian mistletoes are few, and have been concentrated in particular disciplines. Àt the time I began the planning for this project (late 1979), the Àustralian research effort constituted a-bout 25 papers, half of which were devoted to systematics arìd cytotaxonomy or to the control of mistletoe by trunk injections. By comparison, studies of Australian mistletoes have burgeoned Page 3 in the past five years, primarily in the field of reproductive biology (see various chapters in Calder & Bernhardt 1983).
7 .2.7 Biogeography and systematics
About 3100 species of parasitic seed plants are distributed in 18 plant families throughout the world, of which the mistletoes in four families (Loranthaceae, Viscaceae, Misodendraceae and Eremolepidaceae) number 1500 species (Àtsatt 1983a; J. Kuijt pers. comm.). The two rnajor families, Loranthaceae and Viscaceae, are best represented in the tropics and northern hemisphere, respectively (Barlow 1981). Australia has 64 species (11 genera) of loranthaceous mistletoe and 12 species (three genera) of Viscaceae. Various lines of cytotaxonomic, embryological and morphological evidence indicate that elements of the Àustralian mistletoe flora have had varied origins (Barlow 1983). In the Loranthaceae, two primitive root parasites, Nuytsia and AtkinSonig, and a small relictual genus of stem
parasites, UuelICeL¡e, comprise a primitive Gondbranan element. Most loranthaceous species belong to an autochthonous element derived from
Gondwanan stocks, which radiated in the Àustralian land¡nass after final separation from Àntarctica in the late Oligocene. This grroup is characterised by genera such as AByema (36 Àustralian species) which is most diverse in the lowland rainforest and subalpine forests of New GuÍnea and Àustralia but is well represented in drier habitats, and the endemic Australian genus, lysiana (eight species), which occurs across the continent. Both the Gondwanan and autochthonous elements have evolved over a Iong period of time more or less in situ. À third element constitutes the viscaceous mistletoes and a small number of Loranthaceae whose progenitors entered Australia via Indo-Halaya sometime after the collision of the Àustralian plate with the Sunda island arc system in the mid HÍocene (about
15 m.y. BP). Page 4
7.2.2 The mistletoe haustorÍum Parasitic seed plants are distinguished by their capacity to form intrusive absorptive organs called haustoria (Atsatt 1983a). the haustorium of stem-parasitic mistletoes serves a dual function, the absorption of water and mineral nutrients from the host xylem, and attachment to the host. The primary haustorium develops from the swollen tip of the hypocotyl (radicle) of the young seedling. Upon contact with a suitable host branch, the hypocotyl tip flattens against the bark to form a club-shaped holdfast
(Kuijt 1969). From the centre of the holdfast, a wedge of tissue penetrates the host bark and cortex and makes contact with the host xylem. Infection usually causes a hy¡pertrophic response in the host, Ieading to exaggerated xylem production and, externally, a swelling in the branch around the seedling (May 7977: Fisher 1983). In Viscum album, the mistletoe haustorium
becomes embedded in the host xylem during correlated periods of annual
growth (SaI]e 1983).
Hany species also develop secondary haustoria, either from root-like runners which develop from the primary haustorium and grow externaLly along the host branches, or from endophytic cortical strands within the host branch (Kuijt 7969). Hamilton & Barlow (1963) divided Àustralian species of
Àmyema and Lvsiana into two main grroups on the basis of haustorial structure: (1) those in which the primary haustorium is ball-like, sometimes developing aerial shoots from secondary haustoria ("sinkers") in the host wood at the edge of the primary haustorium; (2) species which develop one or
a few longitudinal outgrowths of tissue from the primary haustorium. The
longitudinal wedges grrow against the host wood for distances up to 1 m and
produce secondary aerial shoots along their lengbh. Runners were a-bsent
among the species studied by Hamilton & Barlow (1963).
7 .2.3 Ecophysiology Most stem-parasitic mistletoes are water parasites (hemiparasites) Page 5
(Fisher 1983; Knutson 1983; Calder 1983). The mistletoe obtains water and mineral nutrients from the host by establishing close cell-to-cell contact between the haustorium and the host xylem (Salle 1983). The aerial shoot systems of mistletoes are generalJ.y well developed and appear to fix enough carbon for self-sufficiency (Knutson 1983). Their transpiration rates, both in arid Australia and world-wide, are consistently higher than the hosts', particularly under conditions of water stress (I{ood 7924; Hellmuth 797t; Fisher 1983). The dwarf mistletoes Arceuthobium (Viscaceae) which are parasites of conifers in the northern hemisphere differ from other mistletoes in the tendency towards holoparasitism. The aerial shoot system of dwarf mistletoes is variable in size but generally much reduced. Plants contain about one-tenth the chlorophyll of host plants and provide only about one-thÍrd of their carbon needs (Knutson 1983).
7.2.4 Host specif icity ilistLetoes exhibit marked differences in the diversity and types of hosts which they infect. In Australia, rainforest mistletoes exemplify species with very low host specificty, and occur on numerous hosts of
considerable taxonomic dÍversity (Barlow 1981 ). At the other extreme, there are mistletoes in open forest or woodland communities which parasitise only one species or genus of host. Barlow & t{iens (977) contended that almost aII species in open habitats in Àustralia are host-specific to the extent
that a common or preferred host specÍes or genus can be identified over a large part of the mistletoe's range. Àtsatt (1983a) emphasized the importance of distinguishing between the principal hosts which sustain a mistletoe population and to which the gene pool is functionally adapted, and minor hosts that are sporadically used as encountered. Implicit in the writings of Barlow (1981) and Àtsatt (1983a) is the suggestion that differences in the host "preferences" of sympatric populations of mistletoe are a result of variation in the physiological Page 6 ability of mistletoe species to infect particular hosts. May (197I) demonstrated differences in the susceptibility of hosts to various mistletoe populations of the one species. He conducted experiments in a uniform garden using several populations of two mesguite Prosopis host species and three populations of mistletoe Phqradendron tomenlcsum. Differences in infection success between specÍes, populations and individuals were caused by genetic-based differences in both hosts and mistletoes. Smith (977) documented differences in host resistance between indÍvídual western hemlocks Tsuqg hetgrophvlla in an experimental stand parasitised by ArceuthobiUs tsugense.
7 .2.5 Host mimicry
Some Àustralian mistletoes (Loranthaceae) have leaves whose shape mimics their host (Barlor¿ & lliens 1977). The phenomenon is most obvious in open forest and woodland situations where 43t" oÍ. stem-parasitic species are
highly specific mimics and 352. may be regarded as mimics of one or more of their several hosts. Although known in other parts of the world, host mimicry is most clearly developed among Australian mistletoes (Atsatt 1983b).
Three main hypotheses have been proposed to expJ.ain the phenomenon (Barlow & lliens t977; Barlow 1987; Atsatt 1979, 1983b; Calder 1983), but experimental evidence to evaluate their respective merits is presentJ.y insufficient. t{hatever the causes of host mimicry, the phenomenon indicates that host
characteristics may exert a considerable influence on the mistletoes which parasitise them. Because the host species is a central part of the "habitat" to which a host-specific mistletoe adapts, one can hypothesise that host biology will be a major selective pressure in the evolution of the life history attributes of host-specific mistletoes.
7.2.6 Àustralian mistletoes ard European settlement The densities of several loranthaceous mÍstletoes have increased in parts of south-eastern Àustralia since European settlement (Bríttlebank Page 7
1908; Anderson 7947: May 1941; Beadle 7948; Coleman t949,1950). Population increases have generally occurred in areas directly affected by European
Iand management practices. Calder et q!, (979) observed the tendency for mistletoes to occur where forests had been opened up by timber harvesting, at forest margins, in areas largely cleared for agrriculture, near towns and settlements, and in remnant native vegetation along road margins. A number of factors have been postulated to account for the historical increase in mistletoes in rural districts. Mistletoes are sensitive to fire (Calder et al. 1979), whereas Àustralian sclerophylì.
communities and many desert communities are dominated by plants which are either fire-resistant or whose progeny establish guickly after fires (Gitl et eL 1981). Suppression of fire in rural areas may have led to the increase of mistletoe populations previously suppressed by recument fires
(Hawksworth 1983). Possums (Barlow & l{iens 19771 Barlow 1981) and koalas (Campbell 1948) feed on the foliage of mistletoes, and suffered large population declines due to uncontrolled hunting in the early part, of the twentieth century. SeveraL writers have attributed the increase in
mistletoes to the reduction in herbivore pressure (references in Barlow & tJiens 7977). Anderson (1941) considered that land clearance etas the major factor in permittÍng mistletoes to spread. He argrued that a reduced number of potential hosts subject to a constant seed rain had led to an increase in the density of mistletoes per host.
1.3 EMBRYOLOGY ÀND POLLINATION BIOLOGY IN THE LORANTHACEÀE The Loranthaceae show a number of unusual features in their embryology (Bhatanagar & Johri 1983). Foremost among them is the concurrent development of several embryo sacs in the one carpel. Each four-nucleate embryo sac is produced by two successive divisions of a functional
megaspore. The sacs elongate upwards through the ovary to lie between the Page 8 cells of the stylar tissue. The tips grow up to various heights in the style or stigma, depending on the genus (Fig. 7.2>.In Amvemg, the embryo sacs reach to between six- and seven-tenths of the length of the style. Some or aII embryo sacs may be fertilised after r¡hich the developing proembryos mignate down to the ovary. However, only one proembryo attains maturity, the rest being arrested at various stages of development. Loranthaceous mistletoes generally have showy, hermaphrodite flowers exhibiting a syndrome consistent with bird pollination (Kuijt 7969; Barlow 1983). Outbreeding is the rule in the family, although self-compatibility
may be common and high levels of inbreeding may sometimes occur (Barlow 1983). In a series of papers, Bernhardt and co-workers (Calder et gI* 7979; Bernhardt e! eL 1980; Bernhardt & Calder 1980, 1981b; Bernhardt !982, 1983a,b; Bernhardt & Knox 1983) described the breeding systems of eight
species of Àmyema in south-eastern AustralÍa (Table 7.7). The flor¡ers of aII species pass through five phases which Bernhardt termed Bud, Chinese Lantern Bud, Male, Female and Petals Shed, respectively (Fig. 1.3). Pollen is presented in the dehisced anthers upon anthesis in al1 species, marking the beginning of the MaIe phase of the flower. The petals reflex gradually as the fl.ower ages, increasÍng the spatial isolation of the spent anthers and
stigma (Female phase). Àmvema species vary in the degree of self-compatibility and protandry which they exhibit (Table 1.1). Bernhardt (1983b) deduced that breeding systems of the species s,ere related to their host specificities. Mistletoes with a r¿ide range of hosts were more self-incompatible than those which are obligate parasites of single genera. Fr-¡rthermore, species which parasitised long-Iived trees and shrubs showed a grreater trend towards self-incompatibility than those relegated to short-lived hosts which occur in low density in urrdisturbed natural vegetation. BÍrds are persistent floral foraqers at loranthaceous mistletoes
throughout the world (Keeble 1,8961 Blakely 1922; AIi 1931, 7932; Docters van Page 9
Leeuwen 7954; Kuijt 1969', cill & lfolf 1975; craves 7982i Davidar 1983a). The florat syndromes of the 7 genera of stem-parasitic Loranthaceae in southern Àustralia indicate adaptations for bird pollination (Ford e! ef- 1979; Keighery 1980; Reid 1985*), and a number of field studies have documented bird visitation at fLowers (Sargent 1918, 7928; Àndrewartha t972; Paton &
Focd 7977; Bernhardt g Calder 1980, 1981a; Ford g Pursey 1982; Bernhardt
1984). Excluding some of the flowers of Àmvemg gelaleucqe ç¡hich are sub-cleistogamous, pollination of the flowers of all eight species of Àmvema studied by Bernhardt (1983b) required an animal vector. FÍeId observations of A. pdulum, [- quandanq, À- miquelii, A, miraculosum, À* linophvllum and !- preissii in temperate woodland and forest habitats in Victoria suggested that alt were exclusively pollinated by birds (Bernhardt 1983b). Àt least two species of Loranthaceae are pollinated by insects
(Cammerloher 1921; Hawkeswood 1981 ). Whether insects are consistent pollinators of the flor¿ers of mistletoes exhibiting a bird pollinatÍon syndrome is less clear (Reid 1985). Bernhardt (1983b) observed that, in
addition to honeyeaters, a native bee, Hy]-eoideg conginna, pollinated the
flowers of Àmyemq prej.gsii in Adelaide, South Australía. Insects have been recorded visitÍng the flowers of a number of species of Amvema and Lvsiana, contacting the anthers and stigrnas in some cases (Andrewartha 7972', Paton & Fordt977; Ford et gI* 1979; Bernhardt & Calder 1980, 1981a). Chandran & Suryanarayana ( 797ü considered that the flowers of Dendrophthoe falcata were adapted for Ínsect pollination because honeybees Àpis gglelg were highly effective at triggering the opening of the flowers and collecting the pollen, poltinating the flowers in the process. Neverthless, the flowers of D- lalqela are very símilar to those of southern Àustralian Dendrophthoe which display a bird pollination syndrome (Reid 1985). In view of the uncertainty surrounding the role of insects in the pollination of Australian mistletoes, Ford et al- (1979) proposed that A$yema with open (non-tubular)
*The manuscript of this paper is reproduced in Appendix 4. Page 10 flowers retains the options of both bÍrd and insect pollinators, whereas genera u¡ith tubular or gullet-shaped corollas (e.q- Dendrophthoe and Lvglgng) are more exclusively bird pollinated.
T.4 SEED DISPERSAL OF HISTLETOES 7.4,7 À ç¡orld survey
The fruits of mistletoes vary in length from 2 mm to more than 14 mm, and most contain a succulent viscÍd flesh attractive to frugivorous birds (Kuijt 1969). Few studies have been made of the biochemical composition of mistletoe fruits or of the nutrients obtained by birds which digest the flesh of the fruit. Godschalk (1983a) found that the flesh layer of the fruits of Tapinanthus leendertziae (Loranthaceae) consisted of. 9.17. protein, 34,7% lipid and 47.9% soluble carbohydrates. These values are comparatively high for fruits dispersed by birds (cf. Snow 79711 Stiles 1980; Herrera 798Ð. The energy content (determined calorimetrically) of the flesh was 25,7 kJ g'dry weight. Vlalsberg Q975) fed Phoradendrcn californigum (Viscaceae) berries to caged phaÍnopeplas Phainopgpla nitens (27 Ð. The birds consumed an average of. 264 berries d{, and the energy content which they extracted varied between 26.0 - 28.0 kJ g{ dry weight of flesh. $Jalsberg also examined the value of the succulent berries as a source of water for the primarily granivorous house finch Carpodacus mexicanug (20 g). This species feeds extensively on f, califorEicum berries and other succulent food when nesting in desert areas devoid of surface
water. Caged finches lost weight continuously over 7 d when maintained on a diet of fruit only, but their consumption of 148 berries d{ provided three to four times their daily water requirement. House finches had a higher caloric utilisation efficiency than the frr-givorous phainopeplas when fed mistletoe berries, but could only process enough food to meet 76v. of. their daily enerl¡y requirement. Page 11
Mistletoes are unusual among plants dispersed by frr.¡givores in their association with a distinct set of avian dispersal agents (Snow 1981 ). Throughout the world, birds specialising on a diet of mistletoe fruit have independently evolved several times: the phainopepla in the south-western United States, and perhaps other species of silky flycatcher Ptilqqanvg in Central Àmerica (HcKey 7975: t{alsberg 7975, 7977); the small tanagers of the genus Eunhonia in the Neotropícs (Snow & Snow t97t; Snow 1981); the ç¡hite-cheeked cotinga Zaratornis stEesemanni in the Peruvian Àndes (Parker
1981); some of the Àfrican tinkerbirds Poqoniufus (Godschalk 1983b); certain dicaeids in the oriental and Australasian regions (Mayr & Amadon 1947; Keast
1958; McKey I97Ð; and the painted honeyeater Grantiella picte in Àustralia (Pyke 1980; Liddy 1983; Reid 1985). Specialisation on a diet of mistletoe fruit has proved to be repeatedly successful among birds. In Trinidad and perhaps elseçrhere in the world, epiphytes with similar fn¡its to mistletoes are included Ín the bird-mistletoe system (McKey 1975; Snow 1981). For instance, the tanager Tanqara mexicana feeds preferentially on mistletoe fruit, and the two closely related species, þghyp@ug rufug and L coronetus, on certain species of bromeliads (Snow & Snow 19771 Snow 1981). In the absence of detailed studies of mistletoe dispersal, various
writers have assumed that the specialised mistletoe birds in different parts of the world are the principal seed dispersers of the mistletoes with which they co-occur (Keebte 1896; AIi 7937: Docters van Leeuwen 19541 Keast 1958;
Kuijt t969; McKey 7975; Snow 1981; Parker 1981). The specialised species appear to be the principal consumers of mistletoe fruit where they occur. Moreover, mistletoe fruits dispersed by birds are "soft-seeded", Iacking a hard resistant testa or pericarB. The seeds are often killed if ingested by birds with guts unspecialised for frugivory (Ridley 1930). Birds which specialise on mistletoe fruits show various gastrointestinal modifications, principally in the reduction of the length of the intestine, the increase in the width of the intestinal lumen, and a reduction in the size ard Page 12 musculature of the gizzard (tletmore 1914; Desselberger 1937i Hayr & Amadon !947; Keast 1958; tJalsberg 7975i ÌlcKey 7975). These adaptations speed the passage of seeds through the digestive tract and reduce the chances of the seeds being damaged. In three species of oriental flowerpecker Dicaeum, the gLzzarð. is reduced to a divertículum with a sphincter at the junction of the oesophagus and intestine (Desselberger 1931 ). A similar anatomical condition applies in the Australian mistletoebird D, hirundinaceum (S. bJhite in Gould 1865; pers. obs.). Berries are shunted directly from the proventriculus to the intestine whereas arthropods go into Lhe gízzard for mechanical and peptic digestion (Desselberger 1931 ) ' In temperate regions where specialised mistletoe-feeding birds are absent, bird dispersal of mistletoes has been attributed to less specialised frugivores, such as the waxwings (Bombycillidae) in North Àmerica (HcKey 797Ð, or to a large range of partial or opportunistic frugivores, as in Europe (Kuijt 7969). Recently, more detaiLed studies of mistletoe dispersal by birds have
been reported by Godschalk (1983b) and Davidar (1983a). Godschalk (1983b)
examined the fruiting disptays of three mistletoes in a South African
savannah. The Viscum combreticole population produced moderate amounts of ripe fruit throughout the year. Tapínanthus natalitius (Loranthaceae) fruited for 4.5 mo and ripened few fruit at a time, whereas !- Iegndertziag fruited f.oc 2.5 mo and produced many ripe fruit at once. Four to seven species of bird consumed and dispersed the fruits of each species, but the yellow-fronted tinkerbird Poqsniulus gbgygeconus accounted for 64-94% of the observations of birds feedíng on fruits of each species. Four species of bird, including the tinkerbird, regurgitated mistletoe seeds shortly after ingestion, and deposÍted the seeds on the perch. The mean interval between consecutive regurgitations Ín feeding tinkerbirds varied between 19-43 s, depending on the mistletoe. Thus, although regurgitation presumably caused little chemical or physical damage to the seeds, it r.¡as responsible for Page 13
Iarge numbers of seeds being dispersed close to the parent plant. Godschalk suspected that long-range dispersal in these mistletoes might depend on mobile species of birds, such as mousebirds CoIius indicus, which occasionally ingest mistletoe fruit and defaecate the seeds after a longer retention period in the digestive tract. Davidar (1983a) studied 11 species of Loranthaceae in montane temperate forest on the Nilgiris Plateau, India. One or other mistletoe was in fruit throughout the year, the fruiting seasons of individual species Iasting 2-7 no. The flowerpecker Dicasgs concoloç was recorded taking the fruits of alL mistletoes, and was evidently the sole or primary seed disperser. Davidar (1983a) does not mention other birds ingesting the fruits. À11 mistletoe species had cryptically coloured fruit which were either green or brown when ripe. In half of the species, fruiting was delayed for about 12 mo after flowering, such that ripe fruit s¡ere presented during or just prior to the subsequent flowering season. Furthermore, these species were prÍmarily pollinated by the flowerpecker and had green or brown flowers which the bird forcibly opened to obtain nectar. The nectar was not replenished after flower opening, The other mÍstletoe species had brightly coloured (red, orange, pink) flowers which opened spontaneously, secreted nectar after anthesis, and conformed with a classic bird pollination
syndrome. The flowers were mainly pollinated by a sunbird Neclgrinia mínirne, and ripe fruit production occurred shortly after flowering. Davidar (1983a) suggested that the mistletoes had coevolved with the primarily frugivorous flowerpecker (and perhaps with congeners elsewhere within the range of the ptants) to varying degrrees. The mistletoes $rith cryptic flowers and fruit were both pollinated and dispersed by the sedentary bird, whereas those with brightly coloured flowers were only dispersed by it. The flowers of plants in the former group were considered to mimic rÍpe fruit in both appearance and the type of reward offered, and to have evolved towards attracting the flowerpecker as a pollinator. Page 14
Not aIl mistletoes are dispersed by birds, the main exceptÍon being the dwarf mistletoes Àrceulhobium which have explosive fruits (Kuijt 1969). In this genus, a large pressure builds up within the viscid zone of the fruit during fruit maturation. À zone of weakness eventually gives way, discharging the seed at initial velocities of about 24 m s{ more or less vertically upwards.
7.4,2 l'fistletoe dispersal in Australia
One detailed study of the seed dispersal of stem-parasitic mistletoes has been undertaken in Australia. Liddy (1982a, 1983) studied the seed dispersal of Amyerne camþaqei (Loranthaceae) and Notothixos subgufggg (Viscaceae) in coastal woodland in south-eastern Queensland. À, cambaqei has an annual fruiting season of 2-3 mo, whÍIe the ripe fruits of N- subaureug are probably available throughout the year. The fruits of both species are small and succulent. Mistletoebirds acounted Eor 95% of the 894 mistletoe seeds obtained in faecal samples f,ron 2517 birds (58 species) caught over a 3.5 yr period. Three other bird species defaecated a few seeds and a fowth was seen eating fruits on two occasions. In the field, mistletoebirds defaecated seeds clear of the perch, the seeds falling on to lower vegetation or the ground. Liddy (1983) planted the seeds of both mistletoes which had been defaecated by mistletoebirds on suitable host stems and found that seedlings established. He concluded that mistletoebirds were almost exclusively responsible for mistletoe dispersal at the site. Liddy (1983) and Reid (1985) reviewed the extensive, if anecdotal, literature on mistletoe dispersal in Australia. The available evidence suggests that mistletoebirds and, to a much lesser extent, painted honeyeaters are largely responsible for the seed dispersal of stem-parasitic mistletoes. Both species disseminate seeds by defaecation. The mistletoebird has been recorded feeding on 72 species of loranthaceous mistletoe in four genera (Àmvemg, Lvsiana, Muellerina and Diplatie), and the painted Page 15 honeyeater on five species of Amvema (Reid 1985). In addition to these two species of mistletoe-feeding specialist, at least 18 species of partially frugivorous birds consume mistletoe fruit. Their role in seed dispersal is uncertain. Keast (1958) fed mistletoe fruit to captive silvereyes Zogteropg Iateralis. The defaecated seeds germinated and subsequently established on host stems on which they were deployed. The seeds of À- cambaqei defaecated by an olive-backed oriole Oriqfug eeqlltatUg established when planted on host stems (Liddy 7982Ð. However, À- qambaqei seeds were damaged during passage through the digestive tract of Lewin's honeyeaters Meliphaqa lewinii
(Liddy 1983), and grey currar^rongs Strepera ggfgigqlor regurgitate LvsÍang exogarpi seeds in unsuitable sites for establishment (Brittlebank 1908).
1 .5 THE },f ISTLETOEBIRD The mistletoebird is a small (8-10 g), sexually dimorphÍc flowerpecker (Dicaeidae), which is more or less distributed throughout the Àustralian mainland (Liddy t984; Blakers e! eI* 1984). Most authors agree that mistletoe berries are the staple food of the
mistletoebird (North 1907; Chandler t9t2; Lamm s CåIe-by 1950; Keast 1958;
Chaffer 1966). Some also mention insects in the diet of free-flying birds (CIeIand et el- t9781 tJolstenhoLne 7922; Lord 1939) and nestlirgs (Lawrence
& Littlejohns 1916; Heumann 1926; Littlejohns 1943; Chaffer 7966>. There are only two more detailed studies. Crome 1978) recorded 44 foraging observations over 12 mo Ín lowland tropical rainforest in north Queensland. HaIf of the records erere of birds feeding on fruit or insects in mistletoes, and most of the remainder were foraging attempts for insects amongst foliage. Liddy (982ù mistnetted 108 individuals over 3 yr Ín coastal woodland in south-eastern Queensland, and examÍned 92 faecal samples. The faeces consisted entirely of mistletoe seeds or the viscid fluid associated
with the seeds. Àmyema cambaqei provided the main food between JuIy and Page 16
November when mistletoebirds congregated in the area. Notothlxos ggbaureug
seeds were the main food during the rest of the year when few birds were present.
The specialised nature of the mistletoebird's diet, its pan-continental distribution and its apparent importance as a dispersal agent of Australian mistletoes (section 1.4.2) have prompted suggestions that the mistletoebird and Australian mistletoes have coevolved (Calder 1981; Blakers et sI- 1984). Biogeognaphical evidence suggests otherwise.
The genus Dicaeum (33 species; Mayr & Amadon 7947) and the closely related Ànaimos (6 species) have centres of diversity in Indo-Malaysia which appears to be the centre of origin of their radiation
(l4ayr & Àmadon 7947). The mistletoebird, nominate I hirundinaqeum, is the only species of Dicaegm in Àustralia. Three weII differentiated subspecies of D* hirundinaceum occur on island gfroups (Àru, Kei and Tenimber Islands), each separated by 200-300 km, in the Arafura Sea between Timor and New Guinea (Salomonsen 1961). D- hicundinaceum is closely related to, and perhaps conspecific with (Mayr & Àmadon 7947l- Salomonsen 1961), allopatric taxa throughout Indo-Malaysia. Mayr ( 7944) included D- hin¡ndinaceum in a group of oriental and palaearctic species which he regarded as the most recent immigrants to Australia from Asia. Dr R. Schodde (pers. comm. ) suggests that such species have been in Australia for no more than one million years. Several lines of evidence suggest that p- hirundÍnaceuB may have colonised Àustralia even more recently. The close relationship of DiqgeuB h:lrgndinaceum to taxa in Indo-Malaysia suggests a recent divergence, and therefore a recent origin in that region (Hayr & Amadon 1947). Àustralia ard New Guinea e¡ere connected by a broad land-bridge in the region of the Arafwa Sea ar¡d Torres Strait at the height of the last glaciation, 20 000 yr BP (Nix a Kalma 7972>. D-- hirundinaceum does not occur in New Guinea, so it may not have colonised Page t7
Australia until after the formation of Torres Strait during the Holocene.
The Àru Islands were part of the Àustralo-Papuan landmass during the last glaciation so divergence between D- h- hirundinacggm on the Australian mainland and Q- h- iqnigolle of the Àru Islands has proceeded sÍnce then. The dimensions of L- hirundineceum vary clinally in paÉs of Àustralia but no subspecies are recoginisable (Keast 1958; Salomonsen 1961). The southernmost and northernmost populations vary in size by 5%, which is an unusually small difference for Àustralian birds distributed at both ends of the continent (Keast 1958). Both Keast and Salomonsen attributed the lack of geographical variation to the bird's well-developed nomadic tendencies and the consequent effect of stabilising gene-flow between }ocal populations.
However,.the misttetoebird may not be as nomadic as these authors supposed.
The species is recorded as resident or of permanent occurrence in many parts of Àustralia (references in Reid 1985). Blakers et aI.- (1984) found no evidence of major seasonal shifts in populations in an analysis of atlas data collected throughout Àustralia. Keast (1958) argued that the existence of subspecies of p^ hirundinaceuE on islands ín the Arafura Sea refuted the possibility that the species $ras too recent a colonist of mainland Àustralia to have developed races. However, this argrument is a non sequitur and the possibility that the mistletoebird has not subspeciated within Australia due to the recency of its colonisation would appear to be plausible. Keast (1958) also argued that the mistletoebird was not a recent arrival because of the extent of its "adaptation" to a range of climates within Àustralia. I suggest that the evolution of the genus with oríental mistletoes in Indo-Malaysia pre-adapted the mistletoebird for a coexistence with the diverse Australian mistletoe flora and for inhabiting dry
environments. Among the problems encountered by birds inhabíting $Jann deserts, ç¡ater stress under hot conditions and freezing temperatures may both be important (Davies 7976ù. The mistletoebird's succulent food probably supplies ample water even in hot weather for the bird to maintain Page 18 water balance (cf. gJalsberg 1975). Freezing temperatures are unlikely to be a problem for the species because mistletoebirds become torpid under cold conditions (Heumann 1926). Whether oriental dicaeids have a similar propensity is unknown. Balanced against the evidence that the mistletoebird is a recent colonist of Australia is the fact that stem parasitic mistletoes dispersed by birds have been in Àustralia throughout the Tertiary. The largest genus,
Àmy94a, probably began to radiate in drier habitats with the development of sclerophyllous and woodland vegetation in Australia in the mid to late Tertiary (Lange 7982: Singh 7982). If the mistletoebird was not present, what birds dispersed Tertiary mistletoes? Honeyeaters (ì{eliphagidae) were anong the first passerine families to radiate in Australia, judging from the extent of the radiation and their exploitation of numerous ecological niches
(Mayr t944; Keast 7976), and may have been present in Australia for much of the Tertiary (Ford et aI.7979). They include among their ranks, the specialÍsed mistletoe-feeding painted honeyeater. Other old Australasian passerine families include the frugivorous bowerbirds and birds of paradise (Paradisaeidae) (Maf 7944: Keast 1981). It js likely that these famíIies dispersed Australasian mistletoes and coevolved with them during the TertÍary and early Pleistocene. I suspect that similar arguments to those above prompted Ford et aI. ( 7979) to speculate that the mistletoebird "may be displacing the painted honeyeater" in contemporary Australia, although there is no documented evidence of such a phenomenon.
7.6 THE SPINY-CHEEKED HONEYEÀTER The spiny-cheeked honeyeater is a moderately large (males, 47 gl females, 47 Q, sexually monomorphic honeyeater, distributed widely in inland Àustralia (Boles & Longmore 1984a,b; B)akers et eI- 1984). Schodde Page 19
(982) considers it to have evolved in arid or semi-arid habitats. The Iiterature records the spiny-cheeked honeyeater as eating nectar, insects and fruit, the number of records in each category being approximately equal (Pyke 1980). More detailed evidence of the bird's diet is somewhat contradictory. Keast (1968) said that berries made up a large segrment of the diet and subsequently (KeasL 7976) wrote that the spiny-cheeked honeyeater r"ras "at least 50% frugivorous" judging from stomach contents. Ford 1979) provided the only quantitative data concerninÇ the species' diet, recording foraging observations on nectar and insects in the ratio of 1:1. 0n the basÍs of this and bill size, he included the species in the guitd of long-billed honeyeaters (Ford & Paton t977). At least some of the long-biIled honeyeaters are entireLy dependent on nectar or alternative carbohydrates for their energry requirements (Paton 1982a).
T.7 ÀRID ZONE ''UNPREDICTABTLITY.' AND L]FE HISTORY ATTRIBUTES Effective rainfall is the dominant driving factor for bÍological processes in arid ecosystems, and is often both low and unpredictable (at Ieast from a human perception) (Noy-Heir 7973). Long-term studies at
Koonamore in the South Australian arid zone have shown that biomass
fluctuations aJnong the perennial chenopod and short-Iived species are strongly correlated with rainfall (Nob1e 7977). Peaks in the (above ground) biomass of saltbush Atriplex vesicarie, bluebush MaÍreana sedifslia and the short-Iived species resulted from heavy summer rains (> 85 mm within 30 d) which occurred every 2-7 yr (average 4 yr) in the period between 7926-72, AL
the same time, seasonal patterns of growth are evident among some of the tall sh¡:b and tree species (Maconochie & Lange 7970). The extent to which Iarge rainfall events or a lack of rain influence the amount of leaf flushing during the growing season in species with seasonal rhythms is uncertain. Bioloqists can have preconceived notions about environments with Page 20 which they are not familiar. Harper 0977) pointed out that biologists unfamiliar with the tropics emphasize their climatic stability, while tropical biologists place a great emphasis on the seasonal rhythm of biological events, even in humid equatorial environments. In Australia, biologists often comment on the erratic nature of precipitation patterns in arid areas (e.q. Fleming 7978; various chapters in Barker & Greenslade 1982; Heathcote 1983; Harrington e! eL 1984). This has engendered a popular notj.on that the climate is unpredictable as a habitat for animals and plants in any meaningful sense (Davies 7973,7975,7976a,b), and that the biota have evolved aseasonal (opportunÍstic) reproductive cycles which capitalise on effective precipitation r.¡henever it falIs (Preece 7977; Davies 7976a,b). Davies (7976ù argued that although such patterns have been adeguately documented for a few species of animals, most plants and animals in arid Australia exhibit highly seasonal reproductive cycles. The reproductive cycles of perennial plants in arid areas throughout the world and the influence of rain and soil moisture on their reproduction have been inadequately studied. Some species are reported to flower at any time of the year, depending onJ.y on the availability of soil moisture (references in Mott 1979; Graetz & llilson 1984 for chenopod shrubs).
However, many desert perennials have highty seasonal reproductive cycles.
The Syrian shrub, Haloxylon afliculatgm, flowers annually at the end of summer and fruits about October-November, although flowering is inhibited in a large proportion of the population in dry years (Sankary & Barbour t972). Beatley (7974) reported a 13 yr study of the phenology of plants in the Mojave Desert, southern Nevada. ÀII species $rere geared to the rainfall
regime between autumn and spring, and reproduced annually in spring except
when rains in this period failed. Some shrub species and most perennial grasses and herbaceous perennials flowered sporadically after occasional heavy rains in late summer-early autumn, but for the shrubs at }east, little reproduction resulted. In the Hurchison district, !{estern Australia, Davies Page 21
í976Ð found a remarkably regular calendar of flowering ín 24 species of desert shrubs over a 10 yr period. Flor¿ering and fruiting L¡as seasonal, with one possible exception, suggesting that the environmental conditions ç¡hich initiated reproduction were reqular and predictable. The effects of drought on the reproduction of desert perennials are essentially the same as those exhibited by plants growing in more mesic environments (Mott 7979): moisture stress tends to retard flowering (e.9.
Bykov 7974) and reduces the reproductive output of individuals (Fischer a Turner 7978). Similar responses are better documented for annual plants
(Salter & Goode 7967', Slatyer 1973; Fischer & Turner 1978; Mott 1979). In extremely dry years, perennials in different arid regions of the ç¡orld can fail to flor¡er and fruit, or to fruit successfully (Mott 1979). The important influence of plant water status on reproductive output is suggested by the significant correlations between the amount of rainfall and subsequent flower or fruit production in more than 20 species of arid zone shrubs over a 10 yr period in ttestern Australia (Davies 1968 , 7976b).
1.8 RESEARCH ÀIMS
The preceding sections noted: (1) the notion that birds and mistletoes have coevolved in different parts of the world, and the lack of information of the life hístories of the plants and birds concerned to determine the extent of their reciprocal dependence; (2) the "conventional wisdom" of considering the aríd zone as an unpredictable habitat for plants and animals; (3) the influence of host species on the breeding system and vegetatíve characters of their host-specific mistletoes; (4) the uncertain role of insect pollinators in contributing to the seed set of ornithophilous mistletoes (Loranthaceae); and, Page 22
(5) the prevailing belief that the mistletoebird is the principal seed disperser of Australian mistJ.etoes;
Thus, studies of the mutualism between Amvemg qge¡dgng and its attendant birds were conducted ç¡ith the following aims: (1) to determine the extent of the reciprocal dependence between the plant and bÍrds, and the likely extent to which the evolution of their lífe history attributes have been moulded by their mutualism; (2) to test whether the tife history attributes of plants conform to ¡rredictions generated by the arirl zone "unpredictability" hypothesis, specifically in relation to the seasonality of reproduction and the nature of the breeding system; the predictions are discussed in more detail in subsequent chapters.
(3) to assess the influence of the biology of the host species of A-
$Jg¡dgng as an ecological and evolutionary determinant of life history attributes of the mistletoe; (4) to test the hypothesis of Ford et eI- 1979) that the open flowers of Àmvema are potentially pollinated by insects as weII as birds, and that insect pollinators may contribute to the seed set of plants;
(5) to compare the importance of the mistletoebird as a dispersal agent of A- quqndqng in relation to other frugivores. Table 1.1 species of À¡yema' Breeding system, protandry, seed set ratios and host specificity among victorian From Bernhardt (1983b).
Breeding Àmyema s¡rp Protandrous Seed Host spp system set'
Cgggarina, Eremqphila, Loranthaceae, Self-incompatible À- UffeqUlosum + 0.41 Àqgciq, lyoPorg¡¡, $enlelUn À- pendulum + 0.07 Acac-te, EucalYPlUS, Loranthaceae
Partially self- NAb Arborescent Çaeuarina sPP compatible Interm. 0.28 Arborescent ÇeSgetlna sPP + 0 .56 Porantherous EUgqlvptgg and Àcaqla spp (shrubs and + NÀ Çessia spp (sñi"¡=), [qacla spp understorey trees)
0.72 Two coastal Mglaleuca sPP Self-compatible L mgleleucaC (shrubs A- p¡eisslld 0.46 Coastal fceqiã spp and lot'¡ trees) À- quandeng 0.57 Àcaqic spp Clnrubs and understorey trees)
'Seed set = CÎ fruits)/(i flowers) bNÀ, not assessed -o 'Àdelaide population, South Australia Ð c ta Ì'lorningrbon Peninsula, Victoria o t\) ûJ Page 24
1 htrodrctbn
Fleview
Research aims
2 Study area
3 Mstletoe popdation stnrcttre, dspersion
and dynarnics
4 5 Reprodtrctive plrenology Ecology of the sp¡ny-
of rnistletoes and other cheeked honeyeater pererrials and mistþtoebird
I 6 7 Fruitng display, infection Breeding system and requirements and seed polination ecologry of dispersal of Anryerna q¡anøng Amyerna quandang
I Synthesis
Fiq. 7.1, PIan of the thesis. Page 25
NUYÌSI
NANTHUS LYS ANA
ELYlRANTHE I LLA
Fig. 1,2 Pistil of a generalised loranthaceous flower, indicating the timits of extension of embryo sacs into the style and stigma of various genera. Àfter Bhatnagar and Johri (1983).
Fig. 1.3 Five floral phases of Amyemg qUEEdg. 1. Mature Bud; 2. Chinese mñtern; 3. Hale; 4. Fämale; 5. ÞétãIé She¿. From Bernhardt et gL (1980). CHÀPTER 2
STUDY ÀREÀ
2.7 INTRODUCTION This chapter describes the study area, its climate and vegetation as necessary matters of context for the studies reported in subsequent chapters. The biology of the principal host of Amvema suandanq in the Whyalla region, the western myall Acgc-iq pqg¿gq!!B*, is also summarised Ín view of the hypothesis that host species, as habitats for mistletoes, influence the Iife history strategies of their parasites.
2.2 MIDDLEBACK STATION Middleback station (32o57'5, 737024'E) is 260 km north-west of Àdelaide, near the southern limits of the arid zone ín South Australia (Fig. 2,D, Middleback and adjacent Roopena stations are operated jointly try the
Roopena Pastoral Company. tlool production has always been the main source of
income from the larrd, the first gnazing lease being taken up in 1868 (Noble 797il. Lack of permanent surface water prevented continuous pastoral occupation until the early 1900s (Barker 7972). Lange et e!- (1984) describe the grazing operation and management instituted after 7979. Today, the two holdings are subdivided .into fenced paddocks of 1000-2000 ha, each of which is set-stocked with 200-300 sheep. Under the conservative management of the lessees, bush preservation has been excellent. Despite changes in the population densities of chenopod bush species due to grazing, the vegetation is as close to the original condition as on any lease wíth an equivalent Ier¡gth of grazing history in the South Àustralian arid zone (Lange et al-
ItThe plant taxonomy and nomenclature is that of Jessop (1981) except for the mistletoes and chenopod genera, Rhaqodlg and Chenooodiu8, wtrere Barlow's (1984) and f'lilson's (1983) revisions are followed. These works should be consulted for the author citations. A number of local plant species, such as western myall (or myall), have generally accepted vernaculars in South Australia, and the Engligh names are used throughout the text. Otherwise, plant species are referred to by scientific name. Page 27
1984 ) .
The main study area (about 3 km2) comprised the south-western portion of Overland paddock and an adjacent portion of mid-eastern Railway paddock , 2 - 5 km north of Middleback homestead (Fig. 2.2). Observations were also made in the vicinity of the Middleback Field Centre, adjacent to the homestead.
2.3 CLIMÀTE 2.3 .1 General The climate of the area is characterised by a low and erratic rainfall with no marked seasonal incidence, long hot summers, short cold winters, and a large diurnal temperaLure range. Climatic data are available for tJhyalla (Commonwealth Bureau of Meteorology), 21 km south-east of Middleback homestead on the coast, and for Yudnapinna station (Jackson
1958), 90 km to the north. Rainfall records are also kept at Middleback and
Roopena homesteads by the lessees.
Middteback has a mean annuaL rainfall of about 210 mm, which is one-tenth of average annual evaporation. Total precipitation varies greatly from year to year with no clearcut cycles (Fig. 2.3). The mean nurtber of wet days per month is higher in winter than summer due to the higher incidence of light falls of rain in winter (Jackson 1958). There is a tendency for the heaviest falls to occur in summer. Tropical cyclones move sufficiently far south to bring 80-150 mm of rain over a few days in February in about one in 20 years (Noble 797Ð. Consequently, mean monthly rainfall is distributed fairly evenly throughout the year with a slight pealt in February (Noble 797Ð. l,fonthly totals in any given year tend to be extremely variable (cf.
section 2.3.2) . Mjddleback has a short daylength (sunrise to sunset) of about 10 hr in late June and a long daylength of just over 14 hr in late December. The Page 28 monthly distribution of mean maximum and minimum temperatures at tlhyalla is shown in Figure 2.4. Experience at Hiddleback shows that summer maxima are usually about 4 - 5oC hotter and winter minima 2 - 3oC colder than at t'Jhyalla, due to Middleback's inland position. Thus temperatures in the study area are more similar to those at Yudnapinna, shown in Figure 2.4, than to the l{hya}l.a data.
2.3.2 RainfalI during the study period Fieldwork was conducted between JuIy 1980 and December 1983. Monthly precipitation totals at Middleback homestead between 1979-83 are shown in I¡igure 2.5. Large amounts of rain in L979 and April 1980 produced excellent growing conditions at the beginning of the study, which were maintained by heavy falIs in October 1980 and January 1981. Very litt,Ie effective rain feII after August 1981 and soil moisture declined as the summer progressed.
In March 7982, falls of. t7, 23 and 7 mm on three days each separated by more than a week, provided relief f.or 2-3 mo. However the lack of effective rain across the remainder of the autumn meant that the respite was short-lived. Little or no effective rain feII between April 1982 and February 1983, the
largest daily recording being 5 mm in late May. Extreme drought prevailed by
February 1983, finally breaking with falls of 10 and 25 mm in the first four days of March 1983. Follow-up rains in }ate Harch and April led to improved conditions across autumn, winter and spring in 1983.
The 1982 drought was possibly the worst year of drought in Àustralia this century, droughts of similar severity occurring once in 50 yr (Martin 1983). The l{hyalla region was included in a vast area of south-eastern Australia r¿hich experienced its lowest rainfall on record for the t0 mo to February 1983. Residents of the region considercd 1982 the worst drought Ín living memory. Hundreds of hectares of saltbush died on Middleback and Roopena stations in an unprecedented population decline which was mostly independent of grrazing. Hoç¡ever, the drought was unusual for its brevity. Page 29
The most severe of previous droughts in Australia have usually lasted 2-8 yr
(Martin 1983).
The Middleback records shor¡ that little more rain felI in March 1983 than in March t982, yet the rains in 1983 were drought-breaking in contrast to the 1982 fatls which providecl only temporary respite. The 1983 rains !¡ere highly effective: dams were filled (unlike March 1982), and extensive sheet flow and erosion occurred in the study area and elsewhere on Middleback to a degree not seen between 1979-83. Roopena recorded twice as much rain as Middleback in Harch 1983, so the rain fell patchily across the region and possibly in larger quantities generally than at l'fiddleback. The follow-up rains in late March and early April 1983 enhanced the effectiveness of the initial falls in early March, whereas in the previous year, the three March falls were isoLated in time, diminishing their individual and combined effectiveness.
2.4 TOPOGRAPHY AND SOILS Topogrraphic relief in the region is typically undulating but low, forming a recurring system of interfluvial slopes and plains, and washes and basins. Soils are fairly deep and alkaline. The well-drained slopes and plains car-ry mostly hard pedal red duplex soils or red calcareous earths, and are often grravelly (igrneous or limestone nodules). The poorly drained soils of the basins and washes are typically crusty red duplexes (Laut et eL 1977). In lightly stocked or pristine parts of the lease, a well-developed lichen crust occurs between the perennial. bushes.
2,5 VEGETATION The vegetatÍon of the study area is typical of much of the arid part of north-eastern Eyre Peninsula and is broadly defined as chenopod shrubland
(Crocker 7946; Specht 7972; Boomsma & Lewis 1980). Three vegetation Page 30 formations are widespread: chenopod low open-shrubland, western myall low open-woodland, and smaller areas of black oak Casuarina cristata low woodland (Plate 1). Àll three formations contain a low chenopod bush* cover, between 0.5-1.5 m high. The formations appear to be dj.stributed haphazar:dly with respect to soils and topography. Their distribution in the study area is shown in Figure 2.2. Fire is rare in the chenopod shrublands and the vegetation is not adapted to recurrent burning (Graetz & lJilson 1984). Only two fires have occurred on Hiddleback and Roopena in living memory, and
neither burnt further than about 1 km.
2.5.1 Chenopod low open-shrubland
Chenopodiaceous steppe was formerly dominated by saltbush Atriplex vesicaria in low lying basins and washes, and by a mix of bluebush Maireana sedifolia and saltbush on the interfluvial slopes and plains. Saltbush has clectined under stocking with the result that in moderate to heavily stocked
areas, washes and basins are noç¡ dominated by blackbush Ì'f- pyramidals and the interfluvial slopes and plains by bluebush. Bush species which attain codominant status in partg include Rbaqodie uliqinê, Lycium australg and Àtriplex SËpitata.
2.5.2 tlestern myalI low open-woodland ïlestern nryall dominates a sparse overstorey to the chenopod steppe
across much of the region. It occurs in densities up to 48 trees har in the study area. The woodland tends to be more dense in low lying areas, where species of small tree and shrub may attain local dominance. The most
important are Heterodendrum oleaefolium and ExoqqrBos aphyf]Ug. Scattercd specÍmens or small stands of Eremophile sggpgris, Eqsgle nemonhrle, 9gntefuE
acuminatum, Àcqcia oswaldii, Pittosporum phvlliraeoi{gg and XyoBorun desertorum also occur in wooded areas, most frequently along washes.
*For convenience, 'bushes' are defined as shrubs up to 1.5 m in height, ond 'shrubs' as non-tree woody plants more than 1.5 m high. Page 31 l,fyqporum platvcarcum, a tree to t0 m, sometimes dominates or codominates areas of sparse woodland, both in run-off and run-on areas. Between the tree canopies in woodland, the chenopod bush cover comprises the same species as in low open-shrubland. Hovrever, beneath the tree and shrub canopies, there occurs a specialised flora dominated by the berry-fruited chenopods, fuhy-Laena tomentosa, Rhaqodia spinescens and ChengpgLlg$ qaudichaudianum.
2,5.3 Black oak low woodland Black oak is a clonal species forming extensive groves of thousands of ramets (see the aerial view of a grove in Lange 1969). Occasional trees and shrubs of other species occur within grroves. The bush cover is a heterogeneous mix of bluebush, saltbush or blackbush (depending on the site) and berry-fruited chenopods.
2,6 BIOLOGY OF IIESTERN MYALL lJestern myall is the dominant tree species in the lJhyalla region. It occurs singly or in small uneven-aged groves of. 2-8 trees with contiguous canopies. The woodlands which it dominates are thus a mosaic of grroves and inter-grroves. The species reproduces entirely from seed, recruitment being episodic and coincident with rare flood years which occur about five times per century in the t{hyalla region (Lange & Purdie 1976). Independent estimates of the minimum longevity of the oldest trees are aII greater than
225 yr (CorreII & Lange L966; Lange & Purdie 7976; R.T. Lange, pers. comm.). Six grrowbh stages in western myall were recognised by Lange & Purdie (976) (Fig. 2.6ù, differing in canopy dimensions and shape (Fig. 2.6b). gpen paddock populations display a conspicuous lack of young plants irr stages I-III (Lange & Purdie 7976; Dickson 1983), although grazed seedlings from the last flood year in 1973 are common around the margins of some groves. Recruitment of stage I and II individuals has occurred only in Page 32 favoured sites along bitumen roads, probably due to increased run-off and reduced gnazing pressture. The gap in the age structure of paddock populations represents a lack of recruitment over about the last 75 yr, a period which is coincident with the presence of rabbits and permanent sheep grazing in the region. Page 33
o30 km
Port Augusta
ROOP A lron Kn Katu ¡ e an NSET . E lron Baron hyalla Spencer Gulf Eyre Peninsula
Fig. 2,1. Hap of the l{hyalla region and the location of Middleback and Roopena stations. The heavy broken line approximates the bourdary between the arid zone in inland Àustralia and the seasonally hu¡nid coastal fringe (after Norbhcote and Hright 7982r. Page 34
0 5 km
Dep E te to
ailwa
E NSE illabong edge Corne ver d oO ac paddo o OO ^( h ome ea k &sh fef quart rs
KEY FOR INSET
F.----.< 3.3 km Census traverse
Station road Fenceline
ffi Black oak low woodland Dense western myall ffix low open woodland Sparse low open woodland Wash arrows indicating the direction of drainage
Fig. Z.Z. Location of the study area in Overland and Railway paddocks in relation to the homestead ard other paddocks. 500
400 ^ Ê, e ^ A J 300 ^ l! ^ z 200 a É.
roo
I 960 r 970 r 980 r 930 I 940 I 950
Fig. 2.3. Ànngal rainfall at t{iddleback homestead, 7925 - 1983, in relation to-the long-term average (horizontal solid line).
.E g¡ (a o (,_) U\ 40 Page 36
oo fruJ f F. 20 É llJ fL t-trJ 0 JFMAMJJ SOND MONTH Fig. 2,4. Mean monthly maximum (closed symbols) and minimum (open) teñperatures for tlhyalla ( a, A ) ard Yudnapinna (O , O ). After Commonwealth Buräau of Meteorology, and Jackson (1958).
J FMAMJJASOND
1 979 80
40
1 980 80
E E 40
TL 1981 =fr 40
198 40
40 198
J F M A M J J A S O.N D
MONTH
Fig. 2.5 . Monthly precipitation total.s at Hiddleback homestead, 7979 -7 983. Page 37
(a)
! m Stage 0.5m t age tv
,- -.tÈ-
fi, i.. V í'i Stage
1m 6 I
":ç'i ge ò lll Stage 'l rt vl \ì ,rl
I 2m N
¡
7 (b) ó v
IV 5
E 1 t-x 9. 3 ilt , t¡lT --1- VI ll r 2
+
l2 t3 o 2 3 1 5 ó 7 I 9 t0 il CANOPY WIDTH (m)
Fig. 2,6, (a) Growth stages in western myall (from Lange and Purdie 7976). (bi Canopy dimensions of the growth stages in western myall, showing mean and 952. ðonfidence intenrals (redraern from Dickson 1983). EHÀPIER 3
TIOSTS ÀND POPULÀTION STRUCTURE OF ÀMYEMA QUÀNDANE
3.1 HOSTS, DISPERSiON ÀND ÀGE STRUCTURE 3.1.1 Introduction There is a dearth of information concerning the host specificity and population dynamics of Àustralian mistletoes. Barlow 1966) provided general data on the host range of Australian species of Loranthaceae, and many
writers have commented on the host specificity of local populations of mistletoe (Johncock 7902, 1903; Cleland 7940; Chaffer 1966: Hawkeswood 7979, 1980; Reid 1983; Bernhardt 1983b; Liddy 1983). Thus, we have a general appreciation of the species of hosts which a mistletoe population might
parasitise, but $re are ignorant about whether mistletoes occur on potential hosts at random, what the age structures of the parasite populations are, how long individual mistletoes live for, and the main factors leading to their death or debility. Investigations of the reproductive biology of Aryeng quandanq were
begrun with the premise that the population was actively reproducing and maintaining itself. Early in the study, I thought it was desirable to verify this assumption and, at the same time, investigate aspects of the dispersion of the species which L¡ere possibly influenced by reproductive processes.
Preliminary observations indicated that Àmvema ruandanq seedlings only establish on the comparatively thin stems of hosts. (Subsequent experiments confirmed this - see section 7.3). I therefore adopted the working hypothesis that host branch diameter úras an index of mistletoe age. ReproductÍve status and the number of haustorial branches were also considered to be potential indices of mistletoe age. Empirical evidence for these hypotheses included the fact that seedlings did not produce bud initials and only produced 1-3 foliose shoots, sthereas the largest mistletoes were supported by many haustorial branches. If these variables Page 39 were suitable indices of age, they should be correlated. I also hypothesised that younger mistletoes would be restricted to more distal positions in host canopies than older plants, since the mean diameter of host stems usually decreases with increasing distance from the butt of the tree. This section describes the mistletoes in the WhyalIa region, their host specificities, and the age structure and dispersion of À- quqndanq in the study area. To determine the latter, I measured a number of variables in a large sample of mistletoes in the study area. At the s;ame time I collected quantitative data on the hosts and dispersion of Àmye-rne gqandanq and a second mistletoe species, Lyslang gxocqrpi. My aims were to (1) compare the host range of the tr¡o mistletoes quantitatívely; (2) describe the dispersion
of A* quandanq among the population of potential western myall hosts; (3) test which potential indices of age were most suitable for the mistletoe population; and (4) test whether smaller mistletoes occurred more distally in host canopies.
3.7.2 Methods observations of mistletoes and their hosts were made in different parts of the glhyalla region as opportunities arose. Specimens of host-parasite combinations q¡ere collected where possible.
The quantitative survey of mistletoes in the study area sras conducted in the following manner. A 500 m x 500 m square, designated the trapping area in Figure 2.2, was surveyed and subdivided into 25 one-hectare cells. In November-December 1981, a 10 x 100 m guadrat was randomly selected in each ceII. ÀlI trees and shrubs contained in quadrats and emergent above the bushes were marked, and their height and maximum canopy width recorded.
Two observers working independently carefully searched tree and shrub canopies, as vrell as mistletoe canopies, for misLletoes. Mistletoes $rere
numbered and tagged, and the followÍng variables recorded for each: a) species; b) height of the centre of the haustorium above ground; c) Page 40 radial distance of the centre of the haustorium to the midpoint of the maximum diameter of the host canopy; d) minimum diameter of the host branch proximal to the haustorium; e) reproductive status; and, f) for Ànyeme qualdanq, the number of haustorial branches. Individual À- 9uêndanq exhibited morphological differences in various vegetative and reproductive characters, enabling the branches of plants with haustoria in the same section of host branch to be differentiated. Only individuals r¿ith foliose shoots were included in the survey because of the difficulty of locating young leafless seedlings (see section 7.3).
3.1 .3 Results 3.1.3.1 General observations I recorded and collected five species of loranthaceous mistletoe in
the tlhyalla regÍon between 1980-83 (Table 3.1). Àmyema fl:andanq and lysiana
exoqerpi were the only species in the study area. Amyemq quandEng was abundant throughout the region, chiefly parasitising western myalI. Two of the scattered groves of mulga Acsqia q¡eura on Middleback and Roopena had
light and heavy infestations of Amyemq crueDdanq respectively, but other groves were uninfested. The mistletoe was rarely found parasitising other hosts (Table 3.1).
Amvemg quandang formed eanopies up to 3 m in width and 4 m high when
parasitising western myall (Frontispiece). The Large síze attained by some
individuals was facilitated by the unusual structure of the haustorium. Transverse, Iongitudinal and oblique sections of infected branches showed that cortical strands of haustorial tissue extended from the primary attachment through the host phloem. From the longitudinal strands secondary sinkers penetrated the host wood, and aerial shoots emerged through the bark of the host at points up and down the lÍmb. Individual canopies were thus often subterded by several haustorial branches of varying age (Plate 2). The host branch distal to most À, ggandanq infections supported a healthy host Page 41, canopy, even branches parasitised by large mistletoes.
Lvgianq exocgrpi rras common and widespread in the lJhyalla region, frequently parasitising 12 species in seven families, including Amvema qua¡dang (Table 3.1). L- exoçalpi formed spherical canopies up Lo 1 m in diameter on most hosts, but indivicluaLs up to 2 m in diameter occurredon
Heterodendrgm oleaefollgg (PIaLe 2). The haustorium was invariably a Ìnll-tÍke attachment without runners or cortical strands. The host branches dístal to L gxogarg! plants were usually thin and dead, suggesting that infection rapidly kiIled the host branch beyond the hausto¡ium.
3.1.3.2 Host specificity of mistletoes in the trappÍng area I'testern myall constituted the majority (65%) of the 130 trees and
shrubs sampled in the trapping area (Table 3.2), Five other species occurred in lesser densities, mainJ.y Heterodendrum cleegfolium, lxocarpos aphvllus
and Uycporum Blatvcapgg. Some 534 mistlet.oes of Àmvegs ggandang and lysiana gxgç.qfpi parasitised trees and shrubs or were hyperparasític on each other (Table 3.3). À- qUende¡g had a mean density of 189 ha{ and 5.5 myalla, and accounted for 89% of. the mistletoes. The two mistletoe species exhibited striking differences in host rÐnge and specifÍcity. tJhereas À- quandqng was vjrtually host-spec:ific to western myall, t- gloqarpÍ avoided myall entirely and parasitised every other potential host species except itself and lremonhlla gqonaria. The mÍstletoes dÍffered significantly in the frequencies r¿ith which they were Lryperparasitic on each other, and in the frequencies in which they pa.rasitised other trees and shrubs (Table 3.4).
3.1.3.3 Àmvema guandeng: age indices
The host branch diameters of Arnyeme qugldgnq parasitising western
myalt varied between 2-780 mm (Fig. 3.1) and the number of haustorial branches varied between 1-104 (Fig. 3.2), Half of the population had host
branch diameters less than 16 mm and only one or two foliose branches. The Page 42 sampling period coincided with the post-flowering season and the commencement of the 1982 fruiting season in À- zuaDdanq (section 4.3.1). Reproductively mature mistletoes bearing ripe or developing fruit comprised
522. of the À- quendelg population. Thirty-two per cent bore no reproductive parts, and the remaining 16% bore axillary bud initials but no f¡'uit.
The relationship between the number of haustorial branches and host branch diameter is shown for the three reproductive categories in Figure 3.3. Fruíting plants spanned almost the entire range, from apparently young, single-stemmed mistletoes infecting branches of 5 mm diameter, to multi-branched plants on large limbs. By contrast, most of the mistl.etoes which were non-reprodtrctive or only in bud had less than 5 branches and
occurred on host branches less than 25 mm in diameter. They were presumably young. The few non-fruiting plants which occurred on thicker branches
appeared to be older, retarded or debilitated individuals.
3.1.3.4 ABvegre quanclang infection of western myall ]'he height of western myall canopies was significantly correlated
with maximum canopy width (E = .60, D = 82, P < .001). Larger trees supported more mistletoes than smaller ones (Fig. 3,4), and the linear regressions of the log-transformed number of mistletoes per tree on canopy height and width were both significant. However, the multiple regression on both variables indicat,ed that height djd not account for any variation in
mistletoe numbers over that explained by canopy width (Fig. 3.4).
The bulk of the Àmvgme ggendang population parasitised a sma1l proportion of the potential western myall hosts (Fig. 3.5). Fruiting mistletoes srere more clumped in their distribution than was the population as a whole. Uninfected trees comprised lhe modal class (32%) of hosts (Fig. 3.6). The number of mistletoes per tree did not fit a spatial Poisson distribution, owing to the high degree of contaqion in mistletoe
distribution across hosts (Àppendix 1 ). However, the data fitted the Page 43 negative binomial distribution. A model based on this distribution, using the host canopy dimen.sions as covariates, was derived by M. Morris* & t¡. Venables* (Appendix 1). Mistletoes were spatially distributed thr:oughout most of the canopy of western myalls (Figs 3.7 & 3.8). The virtual absence of mistletoes below
25% of. canopy height (on average, < 1 m) and above 85% (on average, ) 4 m) was due mainly to the limited amounts of canopy at such heights. Myall canopies $rere grazed by sheep below 1-1.5 m and, due to their mushroom shape, had tittle canopy available to be parasitised hÍgh in the tree. Simitarly, the pre¡ronderance of plants midway between the centre and extremity of tree canopies (Fig. 3.8) reflected the distribution of canopy volume. Putatively young plants, i.e. mistletoes which either had small host branch diameters, few haustorial branches or did not bear fruit, tended to be distributed higher and more distant radially in tree canopies (Table 3.5).
3.1.4 Discussion
3.1.4.1 The abundance of Amyema g[le¡delsl
There are references to the abundance of Àmyema qggq{anq early in the history of permanent pastoral occupation in the ÍJhyalla region. tlhite 19tZ) traversed the country west of Port Augusta in 1911 and mentioned the "Iarge bunches of mistletoe which hung from the myall trees". In the Gawler
Ranges, north-west of lron Knob, he commented that "In some places there was hardly a myall tree that had not a large místletoe suspended from its
branches" (tlhite 1913). Bryant (1937 ) commented on the considerable mistletoe infestation of myalIs at Hiddleback in 1936. Considering the relatively minor changes wrought by grazing and European lard management practices generally in the region, it is tikely that the abundance of À-
*Department of Statistics, University of Adelaide. Page 44 que¡{anq then and noç¡ is natural, and not a result of disturbance consequent upon settlement (cf . section 1.2.6).
3.1.4.2 Host specificity
Àmyems ç¡Jendelq was effectively host-specÍfic to western myall, not only in the trapping area but in the region generally. Three of the five species parasitised by À* ganda¡g to a minor degree were also |cagia species (Tabte 3.1). These observations agree with Barlow's (7966) that the hosts of A- quandang are exclusively Acagj.q species. The three other species
of Àmygrng in the region also showed narrow host specificÍties in comparison to L- exccarpi (Table 3.1). Àlthough numerous in restricted parts of the region, these species were not wídespread because of the generally patchy
occurrence of their principal hosts. Àmveme species of woodland and open forest habitats generally exhibit high host specificity (Barlout 1966i
Barlow & ÍJiens 7977>.
t,vslana exocalpi commonly parasitises a taxonomically diverse range of hosts in the one area (Johncock 1903; Brittlebank 1908; Barlow 7963, 7966; Reid 1983). Barlow (1963,1966) implied that local populations of !- exocarg! have a "major" host, the identity of which may differ
geographically. He later commented that almost aII mistletoes of open forest
and woodland habitats in Australia are host-specific, at least to the extent
that a common or preferred host species or genus can be rccognised over a Iarge part of the species range (Barlow 1981 ). However, the concept of a nrajor host in relation to L exacer!! may not be terrable in the Whyalle region. L exggegpi freguently parasitised both Exocarpqg aphvllus and
Àmyenq qUeldelg in the trapping area, and observations throughout the region suggested that, for a given site, it parasitised Íts frequent hosts in the proportion in which they were present. DespÍte the low host specificity exhibited by Lvsiang exoqecul, it did not Ínfect the most aburdant tree, western myall, in the trapping area, Page 45 and rarely did so anywhere in the region (Table 3.1). Tr¡o factorg could account for the disparity in the infection patterns of the two mistletoes.
They may differ in their physiological ability to infect and establish on host species, i.e- !- exocarni can establ.ish on most shrub and tree species except western myal1, whereas Àrnygma quandeng can only infect myalls. Àlternatively, they may differ in their patterns of seed dispersal, i.e. L exoca¡p! seeds are widely dispersed to tree and shrub canopj.es excluding western myaIl, whereas À- guandanq seeds are only dispersed to myall canopies. The chances of such highly specific dispersal patterns occurring seems remote because the two mistletoes share the same dispersal agents (Chapter 5) and one needs to postulate that !- exocarpj. seeds are disper:sed to A- quandang canopies but not to the adjacent myall canopies which À- quanQanq parasitises. However, in an unreplicated infection trial in which i deployed 77 L e¡qcarpi seeds on a western myall, three seedlings established and survived for at least 16 mo. Clear:ly, the reasons for the differing pattern of host infection between À, gUgnda¡g and !, exocarr¡i require further study.
3.1.4.3 Haustorial structure
The haustorium of ÀmvemC SJqndglg on ç¡estern myall does not conform to either of the main structural types recognised by Hamilton & Barlow (1963), but is similar to À- EaidCn!!, an arid zone mistletoe which is also host-specific to Àcacie (Hamilton & Barlow 1963; BarLow 7966). In both
-species, numerous small cortical strands ramify within the host phloem, giving rise to secondary sinkers and aerial shoots along the infected branch. À similar structure is seen in Vlscum afbum of Europe (Thoday 1956;
SaIIe 1983). The evolution of haustoria which spread laterally within the superficial host tissues is correlated with high host specificity (Fisher 1983). Hamilton & Barloç¡ (1963) speculated that haustoria with cortical Page 46 strands or longítudinal wedges evolved in response to aridity because ÀmveBg species possessing them occur more frequently in arid habitats. In support of their hypothesis, Fisher (1983) argued that the lateral. spread of such haustoria provides a larger area of contact with the host xylem, facilitating water upt.ake. However, the correlation between haustorial structure and climate is not clearcut among Amvema species, nor among other taxa as exemplified by the north-temperate Viscum album. An alternative explanation for the evolution of ramifying haustoria concerns the advantage of vegetative persistence on long-J ived hosts. L cruandang parasitising western myalI often outlived its primary aerial shoot system and haustorial connection, surviving as secondary moduJ.es up and down the host branch. The structural connection of the primary haustorium appears
Lo weaken with age, due to the mass of the mistletoe canopy and the convoluted (hypertrophied) growth of the host wood around the haustorium. 0n a slow-growing, Iong-lived tree like western myall, a mechanism of vegetative persistence Ís selectively advantageous for the mistletoe. Hany arid zone tree species are slow-growing and long-Iived (Crisp & Lange 1976;
Crisp 7978i Harrington et al- 1984; R.T. Lange, pers. comm.), which may account for the preponderance of ramifying haustoria among arid zone Àmvgme species. 0n fast-grrowing hosts such as the post-fire successional Acacig species in the sclerophyll forests of south-eastern Australia (Specht 7972), mistletoe death may more likely result from host branch abscission or fire than to senescence of the primary haustorial-xylem connection. Under these circumstances, selection would favour rapid development of the primary. aerial shoot system and rapid sexual reproduction rather than vegetative persistence. Interestingly, A- guandang parasitising short-Iived acacias in temperate eucalypt forest in VictorÍa has a non-ramifying balI-like haustorium (D.H. Calder, pers. comm.). Data relating the haustorial structure of mistletoes to the longevity of their hosts would provide an initial test of the persistence hypothesis. Page 47
3. 1 .4.4 Àge structure of Amyema ganda¡g llhite (1980) cautioned that there sras no substitute for age directly observed in plants if age structures stere to be discussed accurately, but conceded that size distributions coupled with a complete understanding of the bÍology of the species could be helpful. Host branch diameter is the best of several readily measured indices of age in À¡;¿ema ggandO!9, but has several limitations. Young mistletoes establish on western myalI branches varying between 1-16 mnr in diameter (sectj.on 7.3), Ieading to errors in age estimate between plants which establish on branches of disparate size. Site differences between western mya1Is influence their growth rates and presumably the rate of branch girth increment. The latter may also vary, depending on position in the canopy. The rate of girtlr increment of brartches probably decreases with time, as it tends to do in tree trunks (Carron 1968), so an age index based on host branch diameter will be a non-Iinear function of time. À- SandErìg occasionally spreads vegetatively frorn smaller l-o larger branches. Such plants need to be excluded from considerations of population age structure.
The advantage of host branch diamel-er as an index of age lies in its
monotonicity, compared with other easily measured variables. tlhen lmvema qugldanq is retarded or debilitated, it suffers reductions in canopy volume
and number of haustorial branches (section 3.2), or stops reproducing. Thus, young individuals on thin branches invariably have few haustorial branches but older plants on large limbs have a variable number (Fig. 3.3). The onset of reproductive maturÍty appears not to be closely correlated with age either: putatívely young plants on stems as thin as 5 mm bore fruit, whereas
several plants on 20-30 mm branches and with moderate-sized canopies did not (Fi9.3.3).
Host branch diameter is a sufficiently robust index of age in A$yema
zuqndelg to conclude that the population in the trapping area is comprised mainly of seedlings and young plants, and that it is evidently maintaining Page 48 itself. In an actively reproducing population, the dominance of young plants might have been predÍcted on the basis of the distribution of host stems in various size classes. Às trees age, the total length of branch in even-aged cohorts of stems decreases, due to abscission and other loss factors. Assuming that host branches are lost in a random manner with respect to whether they support a mistletoe or not, the number of surviving mistletoes on a given cohort of stems ought to track its dwindling resource through time.
3.1.4.5 Patterns of western myall irrfection
The canopy dímensions of sampled western myalls (Fig. 3.4) tended to be smaller than Dickson's (1983) measurements of stage IV-VI trees in the
same general area (Fig. 2.6Ð. Her selection of trees was biased against individuals with axecl branches (for fence-posts and firewood), heavy mistletoe infestations, or showing suppressed or distorted growth due to the presence of adjacent trees. Hany of the trees sampled in the present study would not have conformed to her selection criteria, accounting for the smaller canopy dimensions recorded here. Larger western myalls supported more mistletoes than smaller trees, Símilar correlations between host size and the number of mistletoes per tree
have been reported by Williams (7977), Hreha & f'leber 1979), Lamont &
SouthalL 1982) and Thomson & Hahalt (1983). Such a relationship would be predicted from a nuII hypothesis of uniform seed rain intercepted by canopies of varying volume. However, two factors complicate such a simple interpretation. First, avian seed dispersers may preferentially seek larger trees in which to perch, rest and feed, biasing the chances of larger hosts towards infection by mistletoes. Second, the canopy size of western myalls declines between growth stages V and VI (Fig. 2.6b). Old trees in stage VI
have been subjected to a longer period of seed rain than young individuals,
and have passed through the growth stage which, by virtue of larger canopy Page 49 size, maximised their chances of being parasitised by mistletoes. Thus, old senescent trees probabty tend to be infected with more mistletoes than young trees of equivalent canopy dimensions.
Àmyema qua¡danq exhibited a contagÍous distribution in relation to íts potential hosts. Contagion is frequently observed jn the dispersion of mistletoes (Room 1973: Smith 1977; Thomson & MahalI 1983; Godschalk 1983b; llemmerly CL el- 7979;Ostry eL eI- 1983). In two instances, significant clumping of mistletoes has been shown to occur as a result of higher recruitment on already infected hosts (Smith 19771 D.C. Paton pers. comm.).
The uneven age structure of the À* quandang population suggested that infected hosts were more likely to accumulate new seedlings than uninfected trees.
Two main factors probably account for the contagion in mistletoe populations. Fírst, the seed shadow of individual mistletoes is often largety restricted to the canopy of the host tree. This is true of both the dwarf mistletoes ÀrceUlhobium which have mechanically discharged seeds (Hawksworth 1961; Scharpf & Parmeter 7977; Hudler & French 7976; Smj.th 79771
Yluir 7977 ) and bird dispersed mistletoes (Godschalk 1983b). The disper:sal of A- ggandanq seeds was biased towards proximity to established plants (sectíon 7.4.3.1). Alternatively, since individual hosts may differ ín their
resistance to infection (l(ay 1977 ), susceptible individuals may accrue a disproportionate number of mistletoes (Smith 1977). The significant relationship between myalI canopy dimensions and the number of mistletoes per tree might be cited as evidence against this hlpothesis because resistant trees ought not necessarily to be smaller trees. However, if host susceptibility is a matter of degrree rather than a dichotomy between absolute resistance and susceptibility, even relatively resistant trees r¿ould tend to accumulate mistletoes through time. Additional hypotheses to explain mistletoe contagion could be postulated. For instance, post-dispersal seed predators miqht be patchily Page 50 distributed, thereby influencing patterns of recruitment, Seed dispersers, in favouring certain trees for nesting or territorial proclarnation, could transfer large numbers of mistletoe seeds to one or a few hosts. However, none of these hypotheses were tested, and the contagion in Àmyema quandang populations and its underlying causes reguire further study.
3.2 DEATH ÀND DEBILITY 3.2.1 Introduction Barlow (1981) likened mistletoes in arid environments to phreatophytes in the sense that they utilise a relatively permanent waten source, in this case the transpiration stream of the host. Histl.etoes both in arid Australia and world-wide have high transpiration rates (t{ood 7924; Hellmuth 7977; Fisher 1983). Barlow (1981) observed that mistletoes tend to die before the host under conditions of water stress, presumably on account of their greater v¡ater requirements. More detailed information on the effects of drought or other factors causing death or debility in mistletoe populations in Àustralia is lacking. I monitored the fate of a large sample of individual Àmyema g¡gndanq and lvsigna exocarpi f.or 2.5-3.0 yr in the course of studies on mistletoe reproductive phenology. The remainder of this section describes the survival of the plants in relation to the drought and other debilitating influences.
3.2.2 Sampling considerations Sampling considerations relevant to work described in subsequent chapters dictated the design of the mistletoe monitoring system. The main aim was to collect data spanning the study period on the reproductive phenology of the two mistletoe species (Chapter 4), which could also be related to bird abundance in the area (Chapter 5). I censused birds using a Iine transect method (section 5.2,2), necessitating that I also sampled mistletoe phenology along the same traverse. The route of the traverse Page 51 intercepted aII the various ç¡ooded habitats encountered in the study area: western myall low open-woodland in both run-off and run-on situations, with
MyoBorum plalvcagpgm codominant in parts; washes, containing a variety of tall shrub and tree speci.es; and black oak low woodland (Fig. 2,2).I sampled large mistletoes only, because they contributed the bulk of the standing crop of nectar and ripe frtrit during the flowering and fruiting seasons. Preliminary observations had indicated that smaller plants s¡ere often not reproductive, or bore few flowers and fruits.
3.2.3 Methods
A 3,3 km traverse (Fig. 2,2),100 m in width and divided into 33 one-ha cells, sras surveyed and pegged with steel droppers in September 1980.
I arbitrarily selected, marked and mapped 4 large plants of Àmvema quandalg per cell by locating the 2 plants closest to the midpoints of the northern and southern boundaries of each ceII. Only large plants with maximum canopy diameters greater than 0.5 m were selected. Due to the variable density of plants, 7 cells scattered along the traverse contained 1-3 marked mistletoes only and the 3 cells in the black oak grove contained none. I used a different selection procedure for Lvsiana exocgrpi. If a
marked Àmyeme quandeg ç¡as parasitized by a suitable f, exocarþi, I selected it for monÍtoring. Otherwise, plants of !- exocarpi were selected in the
same eray as À._ qge¡da¡g. This procedure was instituted to save time walking between marked plants. It only biased the sample of !- exog.agg! slightly towards those parasitising L_ suandanq, because À- qua¡dang $ras both more
common and more evenly dispersed than other hosts. I selected only large mistletoes (Iongest branch exceeding 0.5 m) for the reasons above. I continued to monitor the fate of marked mistletoes which suffered major reductions in canopy volume, although some debilitated individuals no longer conformed to the size criteria for phenological monitoring. Nearby conspecifics were added to the sample of plants as mistletoes died or Page 52 declined in size below the sampling criteria.
3 .2 .4 Results
3.2.4. t Amvema cruandqng 1'he fate of 103 large plants were monitored for the entire period between September 1980 and JuIy 1983. The plants survived, on average, the full 34 mo, despite the fact that four (4%) died. In all, 112 large plants were followed for varying periods, of which six died. Death resulted in one instance from the breakage of a 19 mm diameter host limb by an unknown agent. Ànother was largely destroyed by kangaroo browsing and removal of branches, and died several months later. One died suddenly for unknown reasons, and two died after periods of canopy senescence over 6-9 mo. The sixth plant died as a result of unintentÍonal damage which I i.nflicted on the host limb. All six mistletoes s,ere survived by their hosts. Twenty percent of plants suffered a marked loss of canopy during the
study. HaIf of these sustained losses of at least 5[."a of canopy volume.
Large amounts of canopy loss usually resulted from the death of one or more major haustorial branches. The canopy of adjacent haustorial branches remained healthy. The onset of debility in marked plants occurred mostly in
summer and autumn: 16 of 19 plants either died suddenly or first incurred serious canopy loss due to the death of haustorial branches between December
and May inclusive. Most plants which declined did so during the latter haif
of the study when the drought was most severe (section 2,3.2).
Two plants vrere badly infested by a small coccid scale and attendant small ants leidqqgmex sp. (gp Rx) between Àugust and October 1982, which
persisted for over 6 mo on the plants. One sustained a loss in canopy volume
of more than 50% êcross the summer. The other incumed negligible canopy
*The Australian ant fauna is poorly known, with many species as yet undescribed. Ants were identified by Dr P.J.U. Greenslade, CSIRO Division of Soils, and the names and letters of taxa are those wtrich he currently employs. Voucher specimens r¡ere left with Dr Greenslade, and will eventually be ]odged in the Àustralian National Insect Collection, Canberra. Page 53 loss but many developing infructescences were aborted and mature fruit on the plant were approximately half their normaL length.
3.2.4.2 lysiana exoca4! Seventy-two plants were monitored for the 29 mo between February
1981 and JuIy 1983, and survived an average of 26 mo; 312. died. In aII, 707 plants were followed for varying periods, of which 25% died. Deaths occurred throughout the study, peaking Ín autumn and spring in 1982 (Fig. 3.9a).
Two plants of lygianc exocqrpi parasitic on Amvema quandang died simultaneously with their hosts. The remainder which died were survived by their hosts, À significantly larger proportion of plants parasitÍsing A- quandanq died (43%) than plants on non-Àmvema hosts (132.) (Table 3.6). The death of plants on À- ggendang usually resulted from death of the haustorial branch on which the mistletoe was established. In addition to plants which died, 19% lost most of their foliage during the study and looked close to death. The onset of debility in these plants occurred during the drought, peaking in the summer of. 7982-83 (Fig. 3.9b). Debilitated plants occurred on most species of hosts. Most were probably suffering from water stress, although two low plants were heavily grrazed by large herbivores and one was infested with tiny coccid scale and attendant ants.
3.2,5 Discussion
A quarter of the marked plants of ¿rnyema quandanq and a half of the tyglgng exocar¡i died or incurred major losses of canopy volume. The decline or death of plants tended to occur during the drought in the latter part of the study, suggesting that water stress was at least indirectly responsible.
The response of the two mistletoes to the adverse conditions differed. À^ zugÈng plants generally lost 1 or 2 large haustorial branches, and very few died. The net effect of branch loss ç¡as a reduction in the amount of water required by the mistletoe. Àbout 30% of the original !* exgggrpi Page 54 plants died, many as a result of À- qugldanq branch death. Drought-induced debility in L exocarpi was characterised by a reduction in foliar biomass, presumably through the abscission of leaves, which had the same effect as branch loss in À- quandenq in reducing the plant's srater requirements. Host-related differential morbality among conspecific mistletoes, as with lysiana exocggg! parasitising Amyeme zuendanq and non-Amyema hosts, appears to be unreported, and is relevant to the question of host "quality", and principal and minor hosts (Atsatt 1983a). À. ggan{anq is host to a relatively large fraction of the tygiang exgcalp! population in the study area (section 3.1.3) and, on this basis, could be considered a major host.
However the criterion for recognising principel or sustaining hosts must be the relative contribution to the seed crop made by mistletoes grrowing on different hosts. If the age structure of !- exocarti plants parasitising A- que¡de¡g is skewed towards young plants, the contributíon to the seed crop of the Àmvema-based sub-population may be relatively smal1.
No data are available on the longevity of Australian mistletoes. Barlow (1981) considered that they were relatively short-lived, normally surviving less than 15 yr. The few deaths among the sample of large Amyeme quandang (5%) and Lygiana gxocarpi (11% on non-Amverna hosts) plants over a 2.5-3.0 yr period suggested that both specíes live longer than suggested by Barlow (1981). The vegetative persistence of À- quandang long after the death of the primary module lends weight to this view. I attempted to estimate the longevity of Amyema suandanq using data on the growth rates of western myall stems. Dickson (1983) provided data on
the mean area per stem of western mya1ls in the six growth stages. Lange & purdie 1976) used various lines of evidence to give an approximate age for
each grrowbh stage. From these data, I calculated the mean girth of stems in each stage and plotted the data against time (Fig. 3.10). The graph affords a cnrde estimate of the age of myall branches of varying girth, assuming that branches increase in diameter at the same rate as stems at ground Page 55
Ievel. The largest host branch diameter of À- qualdang measured in the study area was 180 mm (although a few mistletoes occurred on larger limbs). This value corresponds to an age of about 30 yr in Fig. 3.10. This estimate is probably conservative. Díckson (1983) measured total basal area of stems as the circumference of the cluster of stems at ground Level, rather than measuring individual stems. She calculated basal area per stem by dividing total basal area by the number of stems. Stage III trees have a mean of 4 stems at ground level and stages IV-VI have aboub 2,5. Hence, the estimates of stem diameter for each growth stage are inflated, particularly for stage iII. Dickson (1983) also avoided measuring trees with heavy mistletoe infestations, whereas most of the mistletoes which I sampled were clustered together on a few trees. Moderate to heavy mistletoe infestation can reduce girth increment in host trees by up to 55% (Nicholson 1955; Hawksworth 1983). Accordingly, the growth rates of the trees on which I measured brancfr diameters may have been lower than those measured by Dickson. 0ccasional individuals of A- quandang occur with haustoria ramiEying through the massive limbs of old western myalls. In the absence of obvious lateral branches which ttre mistletoe might have spread from, one has to consider the possibility that !- quandeng can persist with its host for much of the lifespan of the tree. Page 56
Table 3.1 Mistletoes ard their hosts in the tlhyalla region.
Frequency of Histletoe Localities Host host-parasite combination'
ÀmvgBg tfiddleback Range, Myrtaceae: miquelii Katunga station; Eucalrmtug socialis* Freguent Tregalana station; half-way between Iron Baron ard l{iddleback Àmvema t{idespread on RooPena; Santalaceae: miraculosum further sor.¡th on Santalum acuminatum* Freguent Middleback in DePot, Extension, RaiIwaY, Loranthaceae: Billabong, l{edge Àmvema quandang Rare Corner ard l{arga paddocks. l.fyoporaceae: lyoporum platvcarpum* Frequent Eremophila IgU+LfoI ia* Infrequent
Vulcan paddock, l.fimosaceae: Roopena; 10 km N of Àcecia burkittiix Freguent Roopena turn-off on Port Augusta-t{hYalla road.
Ànvemq l{idespread in Santalaceae: fl¡andanq region. Exocarpos aphvllus Infrequent Loranthaceae: Lvsiana exocaroi Rarex*
Freguent Freguent Rare Infreguent
t{idespread in Santalaceae: region Exocarpos aphvllug* Freguent Santalum acuminatum Freguent
Loranthaceae: Àmvema rug¡dgng* Freguent
Continued over page Page 57
Table 3.1 contd.
Chenopodiaceae: Chenopgdium nitrar- Rare iaceum* Maireana sedifolia Infrequent** Pittosporaceae: Pittosporum phvllír- Frequent aeoides* Caesalpiniaceae: Cgssia nemophila Freguent
Mimosaceae: Àcacia aneura Infrequent À. bunkittiix Freguent ô. Iicn¡Iata* Infreguent ô. mpurocama Infreguent À. victoriaelÊ Frequent Sapindaceae: Heterodendrum oleae- Freguent foliumx
Solanaceae: Nicotiana qlaucgb Freguent
Myoporaceae: Eromophila alterni- Freguent folig* !. Ionqifolie* Frequent !. oppositifglie Rare E. scoparia* Freguent l,fvopon¡m plelyCgXEJS Freguent !. deserti Rare
* Voucher specimens of the host-parasite combination have been lodged with the State Herbariu¡n of South Australia. *lt Seedlings only. 'Freguent: > 10 records of the combination in the region Infreguent: J 10 records of the combination Rare: 7 or 2 records of the combination only. ò Exotic species. Page 58
Table 3.2
The dimensions of trees ard shrubs surveyed for mistletoes in Overland paddock.
Species No. sampled Canopy Height l'faximum canopy (% oî. total) (m) width (m) 1+ s.n. x t s.e.
Àcacia DaD\¡rocarpg 85 (65%) 4.2 ! s.7 7.4 ! 0.3
Helefedendn¡n ol eaef 9l ium* 23 (782") 2.9 + 0.7 3.2 I 0.3 Fixocar"ogs aphvllus t2 e%) 2.8 ! 0.2 3.4 t 0.3
Uyopozut! platyqeælur 6 (5%) 6.0 t 0.4 5.1 t 0.8
Eremephlta scomrie 3 (2%> 3.3 1 0.3 3.2 ! t.3
EreBophi Iq oppositi fol ia 7 (17") 2.1 2.9
* g. oleeefolium gro$rs in clonal groves of small trees. Ramets (having separate stems at ground level) were sampled as 'individuals'.
Table 3.3
The number of rnistletoes of }Syemg quandans and Lvgianq exocaroi ¡nrasitising trees and shrubs or hlperparasitic on each other in the trapping area.
Host species HistLetoe species Àmyema lvsiana E¡andang exogatpi
Àcacia mpvroqgEpg 470
ExoceEpus 4þyllug 2 28
Heterodendn¡m gleaefol iuD 4
Hvopgtuu pfelyqeEpus 4
Eremophi la gppss;Lti f of iq 7
Àmvema quandang 2.4 Lvsiana gxocarci 1 (seedling)
TotaIs 473 (89%) 61, (1t"¿) Page 59
Table 3.4
2 x 2 Contingency tables comparing the host range and specificity of Ànygma quandanq and Lysiana elocaroi. Yates correction stas applied in aII X2 analyses. The null hypothesis in (a) was that the freguency of hyperparasitism was independent of mistletoe species, and (b) that the frequency of parasitism of different species of tree and shrub was independent of mistl.etoe species.
(a) Freguency of hyperparasitism Mistletoe No. of mistletoes species parasitic on hyperparasitic trees and shrubs on the other
ônvcma querdeng 472 t tysigng exogarp! 37 24
X2 = 776.8, 1 d-f-, P < .001
(b) Parasitism of trees and shrubs Histletoe Host species species Àqcqia lxocagpcs 0ther paDytrocarpq æhvIlus species'
Anvene quenderq 470 2 0 Lvsiene exoqsrpi 0 28 9
X2 = 470.1, 2 d-f--, P < .001
' HelCgedendrum oleggfgllgq, UyepqUUn plelycar¡um and Erengphrle eBpesitrlqlie. Page 60
Table 3.5
The relative heights ard radial positions of AUyema qL¡ardarg in western myall canopies. SarçIe % Relative radial % Relative height size distance
(a) Host branch l,fean t S.E. Mean ! S.E. diameter (mm) (i) 2-77 723 54.7 ! t.9 58.0 t 7 4 (íi) t2-27 lzt s8.6 t 1 .8 55.5 t 1 4 (iii) > 2l 138 48.4 I I .6 50 .8 + 1 4
(b) No. of haust- orial branches
(i) t 125 58.3 t 1 8 55.4 t 1 .4 (ii) z 101 s6.5 ! 2 1 60.3 t 1.5 (iii) 3-6 tzt s3.3 t 1 I 56.3 t 1 .5 ( iv) >6 tti 48.9 t 1 7 51.0 t 1.4
(c) Reproductive status
(i) non re- 749 s5.3 t 1 .7 57 .7 ! t.3 productive (ii) In bud 76 58.0 t 2.1 57.9 t 1.8 (no fn¡it) (iii) bearing 241 52.3 t 1 .3 53.5 t 1 .0 fn¡it Page 61
Table 3.6 Hortality in large Lvsiana exocarti plants monitored up to JuIy 1983, according to host species. The X2 statistic tested the null hypothesis that the freguency of mistletoe sr-rvival was independent of host species.
l,listletoes monitored AII mistletoes monitored from beginning of during survey survey
Non-À¡nyema Amvema Non-Àmyeme Àmyema hosts' hosts hosts b hosts
No. survived 26 24 38 40 No. died 4 18 5 22
)G value, 1 d.f . 5.86* 6.37r,
*P <.05 . The non-A¡rwema hosts comprised Hvooonrm platvcar-oum (7), Hetqfoder¡dî{n oleaefolium (4), Exocaroos aphvllus (9), Eremophila gcomria (7), Sqntalum acuminatr.rn (2) and Cassia nemophila (1). t Non-ÀSygma hosts in addition to those listed above were Àcacia paotrrocaroa (1), M. platvcaroum (1), Exogar¡os gohyIug (8) and Eremophile scoperie (3). Page 62
0.3 o z t¡J =o o., t¡J fr IL u¡ 1 atl 50 r- o.1 1 atl 55 1 at 1 80 ]- J u¡ Ê.
0 o 20 40 60 80 100 'l 20 HOST BRANCH DIAMETER (mm)
Fig, 3.1. Freguency dÍstribut'ion of the host branch diameter of 385 ÀSvema quàndanq mistletoes parasitic on western myall.
0.3
() z o.2 fUJ o l¡J E l! t¡J Þ 0.1 J t¡J fr 1 at71 1 at 104 þ
o -o --- o 10 20 -.fb 30 40 50 60
NO. OF HAUSTORIAL BRANCHES
Fig. 3.2. Frequency distribution of the number of haustorial branches in 470 Amvema quandam plants. 1 v.3 Í=t P.= P-ø P- OF HAUSTORIAL BRANCHES m rf(î c€ NUMBER cto cfú¡. t-F FCf o I 7 6 ft-' \ Yl 5 a I >- Y E ^ l ^ ^ / oi4 ú a + I3 v -- \. a 2 \- -- 1 o o1 2345 6 7 I I 10 11 12 MAXIMUM CANOPY WIDTH.(m) Fig. 3.4. The number of mistletoes (N) on 83 western myalls of varying heíght (xr) and canopy width (x2). Trees are subdivided into 4 ãã["gòriãd: 0 mistlelôes (o); ! or 2 mistletoes (r); 3-6 mistletoes (v); and 7+ mistletoes ( I ). The multiple regression eguation was: ln(N + 1) = -0.69 + 0.14 Xr * 0.18 X2. E = 11.937***, on 2,80 d.f . Significance of partiaf regnession coefficients: Xr NSI X, **. *r(B I .01 nn*p < .001 Ñsl not significant. 100 Page 65 90 U' IU o Þ- 80 TU l- 2 70 oTL 60 l- z 50 ()]U fE tU fL 40 TU l- 30 J f 20 f () 10 o 0 10 20 30 40 50 60 70 80 90 100 RANK ORDER OF HOSTS (%) Fig. 3.5. Cumulative percent of the Àmyema qugndang population accounted for by western myall hosts, rarù-ordered from the largest number of mistletoes supported to the lowest. ÀIl mistletoes (O); fniiting plants only ( O ). o.3 zo UJ o.2 af frt¡J TL UJ l- J 0 1 t¡J fE o I ! trE D o 10 20 30 40 50 NO. OF MISTLETOES / TREE Fig. 3.6. Freguency distribution of the number of mistletoes parasitising 85 western myalls. Page 66 o.2 o z fUJ a [rJ É. LL uJ 0.1 ì t- IJJ fE 0 0 20 40 60 80 100 RELATIVE HEIGHT (7o) Fig. 3.7. The height distribution of 466 Amvema quandqng plants in western myall canopies. Mistletoe heights $tere converted to proportions of the height of the host canopy. o.2 zO tu f ø ut É. ¡J- 0.1 ul tl-l (E o 0 20 40 60 80 100 RELATIVE RADIAL POSITION (%) Fig. 3.8. The radial distribution of. 469 Àmvemq quandanq plants in western myall canopies. The radial distances of mistletoes from the centre of the host canopy were converted to the proporLions of half the maximum canopy width. Page 67 60 (a) t40 x \0o oz o560 (b) LU tr40 t¡l Jk20 l.lt rE o JMMJ SNJMMJ SNJMMJ 1981 1 982 1 983 TIME Fig. 3.9. Hortality and defoliation in Lvsiana exgca:rci.. (a) The Aiãtribution of deaths of. 27 mistletoes between Febnrary 1981 and JuIy 1983. (b) The timing of defolÍation in 20 plants. Plants which were followed from the beginning (unshaded) are distinguished from those subseguently added to the survey (shaded). 600 vt âE e 400 V fr uJ lv UJ ill o so 200 l-lrJ U) 0 40 80 120 f60 200 AGE (yr.) Fíg. 3.10. Relationship between basal stem diameter (from Dickson 1983) ard age of the growth stages III-VI (from Lange ard Purdie 7976) in western myall. The curve was fitted bY eye. CHÀPTER-4 REPRoDUCTIVE PHENoLoGY 0F ÀUYEXA AUÀNDÀNq 4.1 INTRODUCTION Determining which of the potentially Iímitless number of selection pressures have been most important in moulding reproductive schedules in a plant population can be a challenging task (Levin 7978). A number of recent studies have focussed on individual variation in the reproductive traits of natural plant populations, and the relatíve fitness attached to individual patterns of reproduction (Primack 1980; Augsperger 1981; Gross & !'lerner 1983; Schmitt 1983). The approach of such stt¡dies is valuable in two respects. It draws attention to the synchrony (or lack of it) in reproduction among the plants in a population. The approach aJ.so prompts the consideration of the causes of the variation among individuals, which may be genetic, environmental or age-related (Janzen 1978', Primack 1980; Schmitt 1983). Such information may be useful in identifying the selection pressures which have moulded the reproductive schedules in the population. For instance, sporadic and highly synchronised fruiting displays, as seen in mast-fruiting plants, suggest pressures selecting for predator satiation (Janzen 7978), so one might be tempted to look for a seed predator. Conversely, asynchronous fruiting displays among plants in a population could be an evolutionary response to competition between individuals for dispersal agents (Janzen 1979). However, one would be reluctant to accept this conclusion if there was evidence that the variation among individuals lacked a genetic (heritabl.e) basis. Flowering and fruiting patterns in Australian mistletoes have been reported in a number of studies. Paton (979, 1985) measured flower and nectar production in Àmyeme pgNUfUm at Cranbourne, Victoria, over a 3 yr period. Bernhardt (1982) plotted the flowering seasons of six species of ÀUyeng in Victoria from Herbarium specimen records. Reid (1983, 1985) used Page 69 similar techniques to document the flowering and fruiting seasons of common South Australian mistletoes in arid and temperate parts of the State. Paton & Ford (1977), Ford (7979), Crome (7975) and Liddy (1983) also provided qualitative information on the flowering or fruiting phenology of one or two species in each case. This chapter presents the first quantitative account of mistletoe reproductive patterns, and addresses the relationship between flowering and fruiting over successive seasons. The reproductive phenologies of Amygme gganda¡g and seven other perennial species were monitored for up to 33 mo during the study. The additional species were studied because they provided nectar and/or fruit for birds. The results presented here address multiple aims. (1) Individual patterns of reproduction in À* quandgng were anaLysed to determine the degree of synchrony ín flowering and fruiting between plants. (2) The population patterns of flowering and fruiting in aII eight perennial species provided data on the seasonal pattern of flower and fruit abundance for nectarivorous and frugivorous birds. (3) The data were used to test a prediction of the arid zone unpredictability hypothesis that arid zone perennials have evolved aseasonal reproductive cycles in order to capitalise on effective rainfall whenever it falls. (4) The results are consiclered in relation to the climatÍc sequence during the study in order to detect the effects of the drought on plant reproductive phenology. 4,2 METHODS 4,2.1 Measurement of flower and fruit abundance in mistletoes The abundance of flowers and ripe fruit on marked plants of Àmvemg zueldqg and Lygiane exqgerpi was measured along the 3.3 km census traverse. Debilitated individuals which did not conform to the size criteria described in section 3.2.3 were not scored. I recorded the incidence of floç¡ers and Page 70 ripe fruit on plants in November 1980 and February 7981, and the numbers of flowers and fruits per individual at intervals of 1.0-2.5 mo thereafter, until JuIy 1983. Counts were made over 1-4 d. Flowers and fruits were counted if there were less than 50 present. Otherwise the number was estimated by counting between 50 and 200 on the plant and dividing the whole of the canopy by the portion bearing the counted subsample. In the case of Amvema floç¡ers, I counted the number of inflorescences and multipliecl by an estimate of the number of flowers per inflorescence on the p1ant. These methods were imprecise, but independent estimates made over 2-3 d were within 30% and usually within 70% of. each other. The use of a more accurate method (e-g-, see the biomass estimation technígue of Andrew et al-, 1979) was not feasible, due to time lÍmitations. Indices of the seasonal production of flowers and fruits r.lere computed for individual Anyeng guanclanq by summing the number of flowers or ripe fruit recorded on sampling dates throughout bhe season. The incidence of buds was recorded if plants were not in flower, and the abundance of freshly-pecked epicarps and developing fruits was rated to the nearest order of magnitude. The freshly-pecked basal halves of epicarps indicated the recent consumption of ripe fruit by birds (sections 5.3.2.1 g 5.3.3.1). The half-Iife of persistent epicarp bases on pl.ants was less than 4 d, and the small proportion remainÍng after 2 wk was recognisably old. Developing fruits were identified as fruit set either in the most recent flowering period, or in the flowering season prior to the most recent, on the basis of size. If one fruiting season merged into the next, the transition between maturation of the earlier and later season's fruits was recorded. Misttetoes bearing freshly-pecked epicarp bases and large immature fruits r.rere considered to be fruiting or "in fruit", even in the absence of ripe fruits. The assumption was made that all ripe fruit had been recently harvested by birds and that the plant was continuing to ripen immature fruit. Page 71 Primack's (1980) index of flowering overlap, Z, was used to quantify the degree of synchrony in the flowering seasons of individual plants: z = t/s/þ1/{n(n - 7)/2) where a is the number of census dates on whÍch two pì.ants s¡ere flowering, b is the number of census dates for whichever individual flowered for the fewest census dates, and the quantity in brackets is calculated and summed for all possible pa.irs of ¡ individuals. The index has a value of 1 when individual flowering seasons overlap perfectly, and 0 when there is no overJ.ap. PrincipaÌ components analyses of f Lot^¡ering and fruiting incidence (1 or 0) patterns were run using the SPSS program PA1 with Varimax rotation of the initiat factors (Nie e! aI* 1975). The data matrix of flowering scores used plants as variables and the 20 sampling dates between 1980-83 as cases, For analysis of the fruiting patterns a fabricated case of zero scores only and another of scores of one were added, because several plants hacl perfect scores of 0 or 1 for the 20 sampling dates. 4.2.2 Flowering and fruiting in other perennial species I monitored the abundance of the flower or ripe fruit crops in six othrer perennials. Ten or more plants each of lvonorum platycarpum, Exocarpos ephyllug and tlglerodendtuq qleaefqlfum s¡ere tagged along the 3.3 km traverse and the size of their flower or rípe fruit crops estimated to the nearest order of magnitude every I-2.5 mo. 0n most field trips, the standing crops of flowers or fruits of these species and the fruit crops of EnchvlaCnq leUentege, Bhqgedis gpingscens and Qhenqpedius qgudigheg{ianum in the study area ç¡ere rated as nil, Iow, moderate or high. Page 72 4.3 RESULTS 4. 3. 1 Ànyene qgetdeng reproductive phenol.ogy 4 . 3.1 .1 Bud inititiation Bud initiation occurred late in each year, shortly after the flowering season (Fig. 4.1), ÀlI plants Ínitiated buds across the 1980-81 and 1981-82 summers, and flowered in the following autumn or winter. In the summer of. 1982-83, all but two plants began to bud between November and January. gne healthy plant with a ).arge crop of developing fruits had not produced buds by the following July. Accordingly, it could not have flowered in 1983. Ànother plant, heaviJ.y infested with scale and attendant smaLl ants across the summer, delayed bud initiation until April-May 1983, by which time much of the canopy had died and the ants had left the plant. Two other plants initiated buds prior to February 1983, but subsequently aborted them and did not flower in 1983. Both bore large crops of developing fruit and, at times, ripe fruit. One lookerl healthy, and the other was heavily infested with scale, tended by small ants. The latter individual produced abnormally smalI ripe fruits and aborted many developing fruits across the 1982-83 summer. 4.3.7,2 Flowering season and f lower production The AEveSg quandang population flowered annually between 1980-83 in a more or less predictable fashion. The first individuals began flowering in February - March in 1981 and 1982. Virtually aII plants flowered across mid-winter, and the last individuals finished betç¡een October and December (Fig. 4.7), Counts of flower abundance showed the same populatÍon patterns as flowering incidence (Fig. 4,2). The small amount of flowering in January 1982 was due to the production of one or two inflorescences out of season by four plants. Àseasonal production of f lorlers did not occur in the 1982-83 summer (Fig. 4.3). Flowering across the 1982 season averaged 1.3 mo later than in 7981, Page 73 and early flowering in 1983 was almost 4 mo later than in 1981 (Fig. 4.4: Tables 4.1 & 4.2). The delay in flowering between 1982 and 1983 resulted from an increase in the time between bud initiation and first flowering (Fig. 4.1). The rate of bud growth was slower across the summer of 1982-83, at the height of the drought, than in the previous summer. Individual plants varied in length of flowering season from less than 3.5 mo to more than 10 mo, and in date of first recor-'ded flowering by up to 5 mo (Figs 4.7 & 4.8). Àn average plant flor¿ered for over 5 mo beginning in April or May. The flowerÍng span and date of first flowering of individual plants r.rere negatively correlated in both 1981 and t982 (Table 4.3). In other words, plants which began flowering early tended to flower for longer than later individuals. The result was a synchronised pattern of flowering between índividuals, virtually all plants having overlapping fLowering. seasons in both years (FÍ9. 4.9). The degree of synchrony in flowering was reflected in Primack's (1980) j.ndex of flowering overlap. Values for the 1981 and 1982 flowering seasons vrere .97 and .92, respectively. If one considers only periods of strong flowering, when individuals had more than 50% of their peak number of flowers open (Prinrack 1980), the values were .72 and.69, respectively. The maximum number of flowers recorded per plant varied between 5 and 1200. Peak number of flowers was positively correlated with flowering span and negatively correlated with date of first flowering in both 1981 and 1982 (Table 4.3). In other words, plants which produced larger numbers of flowers at their peak tended to be those which flowered for longer and began blooming earlier. Such plants were expected to produce a larger total number of flowers in a season than those which flowered later and for a shorter duration. ÀccordÍngly, the index of individual flower production was significantly correlated with peak rrumber of flowers, date of first flowering and flowering span in both years (Table 4.3). The annual flowering pattern (curve) of a plant is effectively Page 74 defined by the date of first flowering, flowering span, peak number of flowers, date of peak flowering and total flower production. Individual mistletoes had consistent flowering patterns, relative to each other, from one fLowering season to the next. The date of first flowering of individuals in one season was significantly correlated with their date of first flowering in the other two years between 1981-83 (TabLe 4.3). The flowering spans of individuals in 1981 and 1982 were positively correlated, as were peak number of flowers, the indices of individual flower production, and dates of peak flowering (Table 4.3). Individual records of peak flower numbers did not differ signiEicantly between 1981 and 1982 (Student's t = .76, 89 fuf*, P = ,87), and production of f lowers by the population Í"tas similar in the two years (Fiq. 4.2). The flowering incidence patterns of the 79 mistletoes scored for the full 33 mo along the 3.3 km traverse are shown in Figure 4.3. Localised flowering patterns characterising particular portions of the traverse were not evident. Nearby individuals often shared the same flowering patterns, but plants elsewhere along the traverse also exhibited similar patterns. À principal components analysis confirmed that individuals close to each other on the traverse were not separable into clusters sharing similar flowering patterns (Fig. 4.10). None of the five major components highlighted a group of plants which were confined to one portion of the traverse. Individuals representative of the groups at either extreme of the major components were distributed along most of the traverse, as were plants with intermediate factor loadings. The principal component accounted for 64,7% of. Lhe variation and highlighted the disparity in duration of flowering between individuals from all parts of the traverse. 4.3.1.3 Fruiting seasons and fruit production Fruit production in the Amygme quanda¡g population occurred continuously. Mistletoes were either in fruit or bore ripe fruit on most of Page 75 the 20 sampling dates during the study (Fig. 4.11). CoIlectively, the proportion of plants with ripe fruit did not fall below 15% at any stage, and the proportion of fruiting plants never feII below 30% (Fig. 4,72). The standing crops of ripe fruit were generally low: 87% of. all counts made on 79 plants over 29 mo were of I 50 ripe fruits (Fig. 4.13). Relatively few plants contributed a disproportionate amount of fruit to the totaL crop available (Fig. 4.7Ð. Twenty percent of mistletoes accounted f.or 60% of the total of summed fruit production indices. An annual cycle in fruiting $ras superimposed on the population pattern of contint¡ous fruit production (Fig. 4.72). Most individuals bore ripe fruit late in each year, shortly after the end of flowering. Thereafter, the number of plants with ripe fruit declined until the end of flowering in the following year. The seasonal pattern of the number of ptants in fruit was similar to the number bearing ripe fruit (Fig. 4.12>. For most of the study, virtually aII plants in fruÍt bore ripe fruit, indicating that consumers rarely harvested alL the fruÍts that were on offer. However, late in 1980, 7987 and in the summer of. 7982-83, the proportion of fruiting pLants was approximately double the proportion bearíng ripe fruit. Àt such times, consumers çJere removing the entire standing crop of ripe fruit on many plants. Ripe fruit was plentiful in the summers of 1980-81 and 7987-82, subsequentì.y decJ.ining in autumn and winter to an average of about one fruit per plant at the end of flowering when consumers were stripping many plants of ripe fruit (Fig. 4.Ð. In the 1982-83 summer, fruit abundance did not increase to levels comparable to preceding years until after the drought-breaking rains at the beginning of March. Thereafter, ripe fruit remained unseasonally plentiful welI into JuIy. The annual cycle in fruiting $ras reflected in the individual fruiting patterns of the 79 mistletoes monitored for the entire period in Fig. 4.15. Most plants fruited in three distinct seasons, corresponding to Page 76 the three population peaks in fruiting in Fig. 4.12: (1) the 1981 season, February to June 1981, (2) the 1982 season, December 1981 to Àugust 7982, and (3) the 1983 season, February to July 1983 (when observations terminated). However, individual patterns deviated from the general pattern in three ways. Plants failed to fruit in a season, fruited continuously between one season and the next, or temporarily suspended and recommenced fruit production within a season. Nine plants (11%) failed to fruit in one or more seasons. 0f these, one large healthy individuai did not produce a ripe fruit in 33 mo, despite the reguLar winter production of large numbers of flowers. Two healthy plants failed to produce ripe fruit in years after poor flowering efforts. Another faiLed to fruit in 1983 after most of its canopy died. There was no obvious explanation for the lack of fruiting in the remaining five individuals which did not fruit in 1981. AII appeared healthy. Thirty-eight mistletoes (48Ð merged the maturation of fruit fronr tç¡o different seasons. The ripening of fruit was staggered such that as the last fruits of the season matured and were removed, the first fruits of the following season began Lo ripen. This group of plants was responsible for the maintenance of fruit production during the annual period of low fruit availabÍ1ity. Because some plants temporarily suspended fruit maturation in a season and others fruited continuously across two seasons rather than three, only five individuals were recorded in fruit on every sampling date, and twelve others on all but one date (Fig. 4.11). Mistletoes which fruited continuously between 1981 and 1982 also tended to fruit across the 1982-83 interval (Table 4.Ð, More plants fruited continuously between the 1981 and 1982 seasons than between 1982 and 1983. Thirty-five mistletoes (447.) temporarily suspended ripe fruit production in one or tç¡o seasons. Few individuals suspended fruit maturation early in each season (Fig. 4.15) when the rate of ripe fruit production was high (section 7.1.3.2). Most temporarily stopped fruiting early or late in Page 77 each flowering season. The increase in plants which were in fruit partway through the 1982 and 1983 fruiting seasons was due to the simul.taneous reinitiation of fruiting by several individuals (Fig. 4.t2). There was no association between plants which temporariJ.y suspended fruj.ting in a season and those which fruited continuously across two or more seasons, the characteristics beÍng randomly distributed among individuals (X2 = .01, n=77,7dÅ,-,P>.9fD,1/ The index of individual fruÍt production was significantly correlated with the duration of fruiting in both the 1981 and 1982 seasons (TabIe 4.3). In other words, mistletoes with large fruit crops produced fruits over a longer period than less productive individuals. The amounts of fruit produced by individuals in 1981 and 1982 were also correlated (Table 4.3). Thus plants were consistent, relative to each other, in the quantity of ripe fruit produced in the two seasons. The fruiting seasons in successive years differed in a number of respects. The duration of fruiting in mistletoes was more protracted in 1982 than 1981 (Fig. 4.16), the difference being highly significant (Student's I - 6.88, n = 82, P < .001). Plants slere more synchronised in the start of the 1982 fruiting season than in 1983. ÀImost all plants began the 1982 season between October and December 1981. Although some plants began the 1983 season between October and December 1982, the majority began later and a few began as late as March-July 1983 (Fig. 4.77). The date of the onset of fruiting in the 1983 season sras significantly correlated with the date of the end of the 1982 season among individuals which did not merge successive fruiting seasons (r = .43, I! = 50, P < .001). However, a similar relationship did not exist between the 1981 and 1982 fruiting seasons (E = -.05, n = 47, ?=.38). Although plants finished fruiting in 1981 over a range of dates, they commenced fruiting simultaneously in the second geason. There r.tas no evidence of dÍstinctive fruiting patterns Page 78 characterising the plants from particular portions of the traverse. Although two or three nearby individuals along the traverse often shared the same fruiting patterns, plants elsewhere on the traverse had similar patterns (Fiq. 4.t6). À principal components analysis confirmed that individuals close to each other on the traverse did not segregate into mutually exclusive clusters sharing similar fruiting patterns (Fig. 4.18). None of the five major components highlighted a group of plants which were confined to one part of the trave r=".2'/ 4.3.1.4 Relationships between individual flower and fruit production Plants which produced larger numbers of flowers set more fruit. The Iinear regression of individual fruit production on flower production was highly significant after correction of both variables for log-normal distributions (Fig. 4.79). Individual flowering patterns Ltere examined in relation to fruit production which provides a measure of individual fitness, at least in terms of female function. Plants which began flowering later in the 1981 season produced less fruit than groups of plants flowering earlier in the year (Table 4.5), and the comelation between fruit index and date of first flowering was negative and significan+. (Table 4.3). The plants which produced more fruit were those which flowered for longer periods (Tab1e 4.3). 4,3.2 Flowering and fruiting in tysiang exocarpi lyeiana exogarpi displayed annual peaks in flowering and fruiting, the timing and intensity of reproduction varying between years due to the drought. Bud initiation occurred in late spring or early summer prior to flowering in 1982 and 1983 (Fig. 4.20a). Flowering commenced in mid-sunmer in 1981 and 1982, and peaked in autumn, with a small number of large individuals continuing to produce a few flowers across the winter. Flowering commenced 2 mo later in 1983 and was not as protracted as in 1982. The Page 79 proportion of the population which flowered declined Ín successive seasons S.t by a total of about t0 and 40%, respectively.'Plants accumulated developing fruits shortly after flowering began in 1981 and 1982, the first fruits ripening about 2 mo later (Fig. 4,20b). However, there nas a longer delay in the appearance of a standing crop of ripe fruit in 1983. Many developing fruits aborted and a larger proportion of immature and ripe fruit was predated by moth larvae than in previous years, Birds may also have removed earJ.y ripening fruit. This could not be determined because epicarp remains did not persist on plants unlike lmygma ggandang. The proportion of plants with r:ipe fruit peaked in late autumn-winter in each year, and fruiting had virtuatly finished by October. The numbers of plants which fruited in 1981 and 1982 were similar, but declined by 50-70% in 1983. Counts of flowers and ripe fruits (Fiq. 4.21) showed símilar patterns and trends as the frequency of flowering and fruiting plants. 4.3.3 Flowering and fruiting of other perennial species The flowering season of UygpefUn plelycalpUm and the fruiting perÍods of five shrub and bush species between 1980-83 are shown in Figure 4.22, U- platyqarÞug flowered annually over a 2-3 mo period in late spring. L - LL -1 I t Ll +L^ Inctlvlüuals tlowergo lor mosL uE Llle IJUIJUIr1LIUil-! -- ìJ- uruulllr¡¡9^^-.: -- yclr.uu,-^.^: ^l ÞLr^^ u¡rÇ synchrony among individuals ç¡as high. nglerodendfum oleaefoliuE fruíted annually in late summer or autumn. In 1981 most plants fruited abundantly, in 1982 a minority of plants produced fruit, and in 1983 only one stand (genet) was found to be fruiting sparsely. Fruiting üras increasingly delayed each year as environmental conditions deteriorated. Çhenwodium gagdichaudianum and Engbylecne lqnenlogg bore ripe fruit between autumn and spring in each year. The non-ç¡oody aerial shoots of L qaudichaudignUn r¡ither in gummer, so reproduction is probably normally confined to winter. Enchvlaena tomenloge plants in favourable situations bore green (unripe) fruits in some summers so the species has the potential Page 80 to fruit after heavy spring or early summer rains as well as in r¡inter. Rhaqodiq spingscens fruited in summer-autumn in 1981-82, but did not begín fruiting again until autumn 1983 after the drought broke. 0bservations prior to and since the study suggest that summer-autumn is the normal fruiting season. Exocarpos aphÈlus bore ripe fruit much of the time but individuals were often out of phase, resulting in mostly small standing crops. Peak crops occurred in mid winter in each year. The effect of the drought on most species was to diminish or inhibit flower or fruit production in the 6-12 mo period prior to March 1983. The dry conditions appeared to inhibit fruiting in Heterode¡{rUn oleaefolium after the drought broke. Flowering occurred between November 1982 and January 1983, few fruit were set, and virtually all aborted prior to March. Thus, the fruit crop failed because very few developing fruit were available for maturation once conditions ameliorated. By contrast, Rhaqqdig spinescens and Exocarnss ephvllus initiated flowering after the Harch rains and were fruiting by the end of the month, and Enqhyfqene tornenlosa began fruiting in Àpri I . 4.4 UISUUSSIUN 4.4.7 Individual patterns of reproduction in [mvema zugndenq Despite ç¡ide variability in the date of first flowering and in flowerÍng slran, the individual flowering schedules of Àmvema quandanq $rere staggered such that aII plants overlapped in flowering in 1981, and almost aIl in 1982. [- ggq¡dang is facultatively cross-fertile (section 6.I.3.2). Accordingly, natural selection may have favowed individuals which overlap Ín flowering with many other plants in the population, thereby increasing the chances of out-crossing. In the non-drought years of 1981 and t982, peak flowering in the population, i.€- peak overlap of individual blooming periods, occurred in mid winter. Àfter the drought, the peak Page 81 probabì.y occurred in spring. Because of the severity of the drought in 1982-83 and the rarity of comparable conditions, one can assume that peak flowering is not usually displaced from winter. Individual fruiting seasons were also synchronised, 80-90% of the poputation cominq into fruit simultaneously between November-January at the start of the 1981 and 1982 seasons. Thereafter, the proportion of fruiting plants declined due to lapses in fruit production among individuals and to exhaustion of the annual crops. The drought caused a delayed onset to fruiting in the summer of 1982-83, although individual responses varied. As above, however, the rarity of comparable climatic conditions would suggest that peak summer fruiting is general for the population. The relative performance of Àmycne gga¡dang plants ín a number of flowering and fruiting variables (date of first flowering, flowering span, peak number of flowers, date of peak flowering, seasonal flower and fruit production) was preserved between consecutive seasons. Primack (1980) found between-year correlations in the peak flowering date and flowering span of individuals of three insect-pollinated shrubs in New Zealand. He reasoned that the individual variation in such characteristics may be under genetic control or reLated to stable differences between the microsites of pLants (g-g* hosts in the case of mistletoes). Site differences between various parts of the traverse were unimportant in contributing to the variability in individual reproductive patterns in À- quandang. Most of the variation appearecl to be a function of canopy size. Observations indÍcated that flower production and peak flower numbers were positively related to the vegetative size of plants. Thus the consistent flowering and fruiting performances of individuals from one year to the next can only be maintained in the short-term. Large plants senesce and young plants increase in size and fecundity, so the stable patterns of performance among individuals observed in suceessive seasons will change with time.3/ Large plants produce the most flowers, have the largest fruit crops, Page 82 and therefore have the highest fitness. They also flower early. The additional resources available for flowering in large plants may be partitioned both between increasing the size of the flower crop and increasing the rate of bud maturation, thereby bringing the date of first flowering forward. Alternatively, large plants may initiate buds earlÍer than smaller individuals. The precise advantages of flowering early, however, are uncertain. One advantage may be the synchronisation of the peak flowering period with that of less floriferous individuals. À long flowering period may also enable resources to be diverted to fruit maturation during the flowering season, permitting the plant to ripen fruit earlier in the subsequent fruiting season when the chances of fruit removal by dispersers ar-e highest ( secti on 7 .1 .3 .2) . 4,4,2 Patterns of flower and fruit abundance in Amyema suandanq: implicatíons for pollination and seed dispersal The seasonal regularity in fLower and fruit production by À$yema qgandang provided a relatively stable pattern of resource availability which animals could potentially adapt to and exploit, either as pollinators, seed dispersers or predators. Individual flowering schedules elere synchronous to +l-^u¡lG g^uE¡¡9^.'+^-+ +l--+u¡¡uu !¡vweÀ€1^"^- qpv¡¡qs¡¡u9oh,rn¡{cn¡a rtÂowsv rrarralssuu¿4J lrr hiah¡¡¿:¡¡ ntrorvver }hraa nr^ môraa mnnthq in winter, imposing a marked seasonality on resource use by potential pollinators and floral predators. By contrast, fruit abundance was characterised by variable but continuous availability. Two factors led to a degree of asynchrony in individual fruiting schedules which promoted the more even distribution of fruit abundance in time. Fruit production in some plants lapsed for sporadic periods, and larger plants merged the maturation of fruit crops from successive years. Fruit production was usually suspended early or late in the fl.owering season when competing resource demands for producing flowers or the neç, crop of fruit, respectively, were arguably highest. Plants srith Page 83 asynchronous patterns of fruit production may avoid competition for seed dispersers by producing fruits at different times of the year, assuming seed dispersers are present whenever fruit are available. The continuous availability of fruit potentially enabled seed dispersers and fruit predators to exploit the resource permanently. 4.4.3 Seasonality in flowering and fruiting tlith the exception of Exoqgrpgs aphylfus and possibly Enchvlaeng lomentqsa, all the perennial species at Middleback described in this chapter dÍsplayed highly seasonal reproductive cycles, although severe drought delayed the timing or intensity of reproduction in most =p""i""6./ in Ànygnq zuan ang, bud initiation occured annually between October and December, and floweríng probably spans late summer to late spring in most years. Fruit maturation usually begins in late spring-early sumner after flowering, and continues at varying intensities for most or all of the subsequent 12 mo period, depending on the individual. Bud initiation in lygigna exocarÞi aLso occured late in each year. Flowering usually commences in mid-summer and fruiting peaks in late autumn-winter. Flowering and fruiting records from Herbarium specimens of À- SJandang and L. exoqa¡gl (Reid 1985) collected in the southern South Australian arid zone corroborate the seasonal patterns of reproduction in the Middieback populations. Seasonal flowering and fruiting is general among temperate populations of Ioranthaceous mistletoes in Australia (Paton & Ford 7977', Ford 7979i Bernhardt 7982; Reid 1983, 7985; Paton 1985), and characterises at least some arid zone species (Reid 1985). The reproductive cycles of most mistletoes thus appear to be geared to an annual regularity in the environmental conditions which initiate flowering. [vong¡um gþtvcarpum and Helergdendrun oleeefolium reproduced seasonally, flowering in late spring and early summer respectively. Fruiting in H, gþgefotium began in January under favourable conditions in 1981, but Page 84 was delayed by drier conditions in subsequent summers. The summer-deciduous ChenonodiuU qqUdichaudia¡um reproduced in winter, being dormant in summer. At the other extreme, Exoqarpog aphyllus bore fruit in a semi-continuous and aseasonal manner. The interaction between season and rainfall in regulating reproduction among individuals of this species deserves more attention. Rhaqodia spinegcens and perhaps lncþylaena lgnentoge produced fruit seasonally, but possessed more flexibte reproductive cycles than I platygq¡pum, H- glea.eJoliuB and the mistletoes. 4.4.4 Effects of drougftt on reproductive phenology A number of trends and aberrations in the reproductive phenology of bhe perennial species, above, $rere inferred to be drought responses on the basis of correlation with the trend in environmental conditions during the study, Such evidence is weaker than the results of controlled field experiments or 'natural' experiments (Erwin 1981), However, literature information on the drought responses of arid zone perennials in relation to reproducbion is similarly empirical (see section 1.7). The deteriorating conditions during the study affected Àmvema qua¡dang reproductíon in a number of ways. Flowering was 1 mo later in 1982 ancl 4 mo later in 1983 than in 1981. The delay in flowering in 1983 was a function of slow bud growth, which probably caused the delay in 1982 as weII. Àt the height of the drought, a smalL number of plants either did not come into bud in late 1982, or aborted all buds prior to flowering in 1983. Individual fruiting seasons were longer in 1982 than 1981, fewer plants merged the ripening of successive fruit crops in 1982-83 than in the previous year, and the start of the 1983 season was staggered between plants in contrast to preceding seasons when fruiting began more or less synchronously. Paradoxically, the most dramatic effect of the drought on ônyene qgeldenq reproductive phenology was the 4 mo delay in the comfnencement of flowering in 1983, long after the drought had broken. Page 85 Much of the delay in flowering in 1983, relative to 1981, occurred after the rains in early March. The slow rate of bud development preceding the 1983 flowering season may have been due both to water stress prior to March, as well as to the dj.version of resources into fruiting after the rains. The standing crop of rípe fruit was atypically low across the 1982-83 summer but promptly increased to normal summer levels in Harch and remained unseasonatly high into JuIy. Maturation of the bulk of the 1982 fruit crop appeared to take precedence over flowering after the rains, diverting resources from bud growth at a time of the year when the previous year's fruit crop is usually largely expended and resources are allocated to bud development. It is uncertain r¡hether the increase in the duration of individual fruiting seasons in 1982 was drought-related. Fruit maturation might have been retarded due to moisture stress, leading to longer individual fruiting periods. Alternatively, the 1981 fruit crop could have been smaller and thus di.ssipated more quickly than in 1982, The data from the traverse marked plants cannot resolve this question. Measurements of standing crops of ripe fruit do not index production because of variable removal rates by birds. Comparison of fruit production indices (based on fruit counts) between years was not val.id because of the different number of sampling dates and the possibility of variable rates of fruit removal by birds between y"ur".l'/ Comparison of the fruit production indices among indivÍduals in one season was valid because plants appeared to experience more or less uniform removal rates. Interestingly, flower production showed littIe variation between 1981 and 7982, Monitoring of plants was not continued past early flowering in 1983. However, subsequent observations índicated that flower abundance was not markedly depressed compared to previous years. Although it is possible that hemiparasites, utilising the transpiration stream of a host, may be buffered from the effects of the drought, reproduction in tygiqna Page 86 gxocarpi was markedly affected in successive seasons. Thus the resilience of reproductive effort in A- quandanq in the face of environmental exigency a must be attributed to either physiological specialisation in the mistletoe or to the combined physiologies of host and mistletoe. The effects of the deteriorating conditions on lysiana eðocarpi reproduction were a reduction in the fraction of plants which flowered and fruited, particularly in 1983, reduced flower crops in successive years, and a marked reduction in the standing crop of fruit in 1983. The drought-impaired reproductive performênce of the population $Jas most obvious after the drought had broken, although the Iow standing crop of ripe fruit was partly attributabte to abnormally high fruit and seed predation by moth Iarvae. The pattern uras repeated with ggteredc¡drum gleaefellun. Although the post-drought conditions in 1983 srere amenable to fruiting, the crop failed because of events earlier in the annual reproductive cycle at the height of the drought. By contrast, the chenopods and Exogarpog ephvllug with short reproductive cycles responded almost immediately to the improvement in conditions, producing fruit within 1-2 mo of the initial rains. The latter group might be thought of as opportunistically reproducing desert perennials. The mechanistic basis for the disparity in post-drought response between the 'opportunistic reproducers' and 'post-drought sufferers' is probably related to three key factors: (1) the timing of the drought and subsequent amelioration in conditions in relation to plant reproductive cycles; (2) the length of time between bud initiation and ripe fruit production; and, (3) the seasonal period in which bud initiation can occur. The post-drought response of the opportunistic reproducers can be interpreted in relation to these factors: (1) the amelioration in conditions occured at a time when they were physiologically capabl.e of floral initiation (summer-autumn for Rhaqodia gpinescens, any time of the year for Exocarpos aphyflUg and possibly Enchvlae¡e lomgntosa); (2) floral initiation Page 87 in these species is probably indeterminate, enabling them to continue to bud in season whenever soil moisture is adequate; and, (3) the time between bud initiatÍon and fruiting is short. By contrast, the span betç¡een bud initiation and fruit production is much longer in Àrnyema quandang, Lvsia¡e gxscarp! and Hetercdendrug qleeefqllg4, and bud initiation is probably determinate or at least fairly precisely restricted to one time of the year. Thus the heÍght of the drought affected bud growth and fruiting in L. zualdq$L the amount of bud initiation and bud growth in Lysiana exocarp!, and fruit set in fl* olCqefolium. Due to the length of their reproductive cycles and their inability to initiate flowering when conditions ameliorated, the effects of the drought on these species were evident long after the drought broke. Page 88 Table 4.1 The median dates of first flowering, peak flowering and last flowering of marked ÀByege qge¡detg plants between 1981-83. Estimated dates are based on interpolations of Fig. 4.5. 1 981 7982 1 983 Hedian date Difference Difference (d) (d) First flowering 22 ltatch 14 April 15 JuIy 23 92 Peak flowering 8 MaY 2 JuIy 55 Last flowering 13 August 20 Sept. 38 Table 4.2 Dates of the guartiles of flower production of marked Àmvema E¡q¡çlanq pl.ants in 1981 and 1982. Estimates are based on interpolations of Fig,4,6, Cumulative freguency 1 981 7982 of flower production Difference (d) 25Y" 12 April 13 May 31 507" 2 May 18 June 47 75% 3 June 22 JuIy 49 Variable Varíable First Flowering Pealt First Flowering Peak Flor¡er Fruit Fruiting Pealt f lowerir¡g flowering span f lor¿ers flowerirEt span flowers production production span 1981 L982 date 1981 1 981 1981 1981 7982 7982 1982 1981 Flouering -.677**x span 1981 (85) Peak flowers -.420*** .405*** 1981 (85) (85) First flower- .513*** íts 7982 (82) Flowering .393*** -.622xx* (95) span 1982 <82) .509*** -.503*** .444*n* Peak flowers (95) 7982 (90) (95) flower . 31 2** .431*** First (92> ir¡g 1983 (79) Flower prd- -.602*** .619*** .826*x* uction 1981 (85) (85) (85) q?7x** Flor¿er prd- -.579*** .520*** .872x** (95) (95) (95) (82) uction 1982 .795*** .571*** .900*** Fruit prd- -.394*r* .426xxx (84) (84) (97) uction 1982 (84) (84) .866*** Fruitirg (85) span 1981 .648*** Peak flowerir¡g (85) date 1982 Page 90 Table 4.4 The number of marked mistletoes of Àmvema quaDdanq in which successive fruÍting seasons merged. t98t - 7982 seasons merged Yes No 1982 - 1983 Yes 15 8 seasons merged No 15 39 ß =8.00, 1d;[-=1. P<.01 Page 91 100 r +--+-c_ r -z\---t I 50 o o o D o o AJ 80 I a2 83 TIME Fig. 4.7. The proportion of marked Àmveme SJÐdsDg in flower (-rr) and in bud or flower Êe) between 1980-83. The average sample size of plants was 92. 250 2 oo t-z J fL 50 U)(r r50 m t¡J o z ,r'l z o l\ 40 =J ,r ,l I lr l\ \ À o l! r00 /\ \ 'n I t,l i'¿ 30 o \ I f, ta \ I t o I I m z I \ I 'n z I 20 ¡ 50 I -1 I c LU I t2' I I l/ I to =(D I I I T I _J I t- b- o o {z 80 8l 82 83 TIME Fig. 4.2. Mean number of flowers (+) and ripe fruit C+-) per plant of Amyema E¡andenq along the 3.3 km traverse. The average sample size of plants was 92. Page 92 Okm I - - E I - I o U) 0) J (ú o o - E - co) o(ú o o. õ E c c .9 (ú 'õ o o o o. - -o E 0) I- Ec) o I .Y C (ú Ø c) o o Ø (ú : = frCÚ 3.3 km NJ MMJSNJM MJSNJMMJ 1 980 1 981 1 982 1 983 Fig. 4.3. Estimated flowering seasons of 79 Àmvema quandanq plants distributed along the 3.3 km traverse, between 1980-83. 100 Page 93 FBo at) l-- z 1981 1 982 ùJ 260 æ t¡l 3 o J lt b40 1 983 oz trJ ol l!H20 o JFMAMJJASOND TIME Fig. A.4. Comparison of the flowering seasons of marked plants of Amvema E¡andanq between 1981-83. 100 -.4 I f r I I I 90 I i I i I I , I 80 I I I f I I I 70 I I I I g60 I l I i o I ì 50 I it I I :) I o I H40 I i ¡ l! I I I I ! I 30 I , , I t ! 20 t I I , I I I I I t , 10 I I I I ) J I o t A A o D A A o D A t 1 1 980 1981 1 982 983 TlME Fig. 4.5. Cumulative proportions of Àmvema quandarìq in f lower,at varying stáges through the flowering seasons in 1981-83. First recorded flowering (-A-); peak flowerirg (+); Iast recorded flowering e'F). Page 94 roo 90 a 80 l- = J 70 È Éat l¡J 60 oÌ J L E o 50 o 2 z 40 l¡Jt l, =l- 30 )J t= o 20 to o N D f^ 5 o N D MJ IA s o N oJt M 80 8t 8? 83 TIME Fig, 4.6. Cumulative distribution of the mean flower counts in marked plants of Àmyeme suandanq in the 1981 ard 1982 flowering seasons. o.8 t98 I (rÞ8 5) o.6 > o.4 o 0.2 e^ ()O z 5 '.o o r 982 LrJ (r:95) ff o.t t¡J o.. kJ frIU 0 .4 o.2 o o 50 r oo I 50 200 250 300 FLOWERING SPAN (DAYS) Fig. 4.7. Distribution of minimum flowering spans of Àmvema quandang in 1981 ard 1982. Minimum floweríng span eras the number of days between the first and last recorded flowering dates. Page 95 2.2 2.O t.8 ô 6 ct l¡l É. L a t.4 (n.8 6) E Ø t.2 ôl¡J o t.o UJ oJ l¡J Ë, (n=95) lÀ I l¡J ¿ t- (n= I 02) J 6 l¡l G 4 2 o DFA A o DT AJAO DFAJ 80 8t 8Z 83 TIME Fig. 4.8. Frequency distribution of the date of first recorded flowering for marked Àmyema cruandgnq plants in 1981-83. Àrea of the bars Ís proportional to freguency. Page 96 1981 1 982 JFMAMJJ ASOND TIME Fig. 4.9. Irdividual flowering spans of Àmyema suandanq in 1981 and 1982, arranged in order of first flowering date. Bars indicate minimum floç¡ering spans between the dates of first and last recorded flowering. Peak flowerirrg dàte is indicated for plants with ¿ 100 (O) and < 100 flowers (O) open. Page 97 0.9 .8 34 37 52 .19 0.8 .42 55 .70 .17 .51 .35 o.7 .40 .l 15676 .16 .54 .58 0.6 .25 .28 .12 44 .33 6l '"" a t/ 1o.r" 39 65 .38 79 0.5 92659 .57 .68 o¡ .50 ,29 l- o.4 .6 43079 z ,3 '41 't ul .5 a,7 .69 z .46 .67 o 0.3 .27 32 49 77 À .36 66 .23 45 7l .63 '62 o .53 75 '43 o o.2 '47 'zl .73 .48 .74 0.1 .64 .l 3 .18 '2O'14.6O .lO o .31 -0.1 .15 -o.2 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 COMPONENT 1 Fig. 4.10. Relative positions of the 79 mistletoes in relation to the first twó princÍpal components summarising flower incidence patterns. Consècutively numbered plants were adjacent on the 3.3 km traverse. Page 98 J? (a) In Fruit to I 6 4 U) 2 zl- fL o ol.L l2 (b) Ripe Fruit o z ro I 6 4 2 o o 2 4 6 I 10 t2 t4 16 l8 20 NO. OF SAMPLING DATES Fig. 4.77 Freguency distributions in Àmveme cruandang (n=79) according to the number of sampling dates between 1980-83 in which they were (a) in fn¡it, and (b) bore ripe fruit. Plants were sampled on 20 occasions. ¿i It ICI TJ lC v. lr- loq Þ,q FREOUENCY(S) l-l . ¿' to. Þ N(J5(,d)\¡@(oO loÀt5. p. ooooooooooo E¡ }A JF5 (¡) Êrù È- rt. @ p RELATIVE FREQUENCY (%) a o 0 JlJ -, (tõ ñitFJO ü¡o N (¡) à (,l o, c .'A o o o o o o o P.b É ctõ OJza o rto ,f\io ìJ It o oP'iù 3[ ¿u¡ (tl trJo 3tFl o o ÞP- rto FJ If €Fñ oc oìJo o 1+ 3 t-' (+ P' o o zo F¡5 -{ 0 =oOJ \OÊ ø 9 æ(n m (*)]ro o = ñ r-ñ od-11 ærñto 0 (^) oF .t> ñP' f, IJ l= oo ! 1\) k o lo cFh mo l= (D Jõ -r1 0 tÞ N aP-ic AJ C+ Cre t3 o ctt ls rño ='o lÈ o o to < |-.Jac l5 ¡-É G) E¡ \... I, o tt o Fñ o o õo tr \_ É,J FJ P- P. rf\¡ Cl) a tfl \O (tlo a t> FJ Klã P. lo ì5 (! lã o u -o tÊ 11ì FJ o c, rO P. o rf \.O \o Page 100 32 a 24 oz u.l oD EUJ 16 l! UJ E UJ E 8 tt o o 2 400 600 1 100 FRUIT INDEX Fig. 4.1A. Freguency distribution of the 1982 fruit production index for 98 Uíå*. qua¡danq. Not shown are the 4¿ oî. plants which had indices of 0. to U) zt- J fL 5 l! o öz o NDJfMAM J ) AS OND F MAMJ J A s ONDJ TMAM )J 80 8l a2 83 T!ME Fig. 4.15. The number of plants of ÀBJeme quqDdeng which suspended fruiting at different times between 1980-83. .0 km I:I - I== -=:Ir¡ :----r -l =::r I::r o ::I - ü, o (d :--: :::- l¿ I o co) o - o Eo 6 (ú c o. : : ::IT o ]C '-u, E (ú o o. o -o o I:=: ! o o E r o -:::::- I I -:¿c -- (ú :- r (t) o - o - -::: o - - I :::-:--=I .u) CÚ I:::I ====r - 'õ= É. 3.3 km N JM M J S N J MM J S N J M MJ 1 980 1 98 1 1982 1 983 Fig. 4.16 Estimated fruiting seasons of 79 Ànyemg qgendgnq plants. Solid bais r"p.esent periods in which plants were in fruit. Open bars represent periods of temporary suspension of fruit production within a season. E A FIRST FRUITING SECOND FRUITING THIRD FRUITING SEASON SEASON SEASON D F A J A ODF A J A o D F AJ 80 BI B2 8õ TIME Fig. 4.77. The duration of non-fruiting periods between successive seasons in Amyema E¡eIdgDq. Bars show the interval in which ripe fruit production 1981 and 1982 seasons and (B) the 1982 and b"tr.¡een a¡t the fruiting -o "".""d1983 seasons. The non-fruiting spans of plants are ranked ín order of the Þ ta start of fruiting in the sgbsequent season. Plants which merged fruiting in o successive seasons are not shown. r¿ O N) Page 103 21 3031 3246 47 67 69 77 0.8 83664 27 37 a 6t a 38 22..6 I rg zg. 0.6 74 2g a 52 J. gg 53 5 t6 42 24 a o.4 t4 t8 63 49 72 4t 45 70 55 a 29 23 l- 40 35 z 3 I 1¡I 78 34 a 44 a 66 z z o.2 a 5p 54 o 5 I 25 68 62'.lQ fL zõ I ¡ ló 7t2 a a o 76 5.8 433 o a 33 po 20 7t a s.p7 5 0 48 65 56 75 a I 50 -o.2 -o.4 73 -o.6 -o.2 0 o.2 0.4 0.6 0.8 COMPONENT 2 Fig. 4.18. Relative positions of the 79 misttetoes in relation to the first two principal components summårising fnriting incidence patterns. Consecutively numbered plants were adjacent on the 3.3 km traverse. I 200 a x l¡l ô a = 600 a E a f a fr a a u- a a a a a a a a a a a aa a aaa a o a l¡ a a aa a ¡ a a a o ...!":'.' :i'" "'! . a o 500 r ooo I 500 2000 2500 FLOWER INDEX index ard 1981 flower irdex -Ú Fig. A,tg, The relationship between 1982 fruÍt þ in-À¡nvema quardans. The tinéar regression of In(fruit ir¡dex + 1) on q n 84, P < .001. o fntfñîer iñext was highly signiiicantt Ë2 = .632, = IJ ÀO a Èt{ gto'f, o H.=lx ts- cr rt O,lO Q ¿!r lo. o l--lo o ÈJll-J À JO lrl . RELATIVE FREOUENCY (%) ( Ef lr'¡r¡ oo c o J è (¡ Crt -¡ (o o \¡Ho.o. 19 (¡t à(¡d,{@eA l\) o o to H o o o o ôõooooo o o o ooo \¡ìJ O O @t--õ J Fil 5 lQ:t (- Fñ O I =l.QtJ.ø o oF T'ÈitFñ |-oorrF € o ö = -ì oõFJc.rQ I rtF.- . C OìC,1 Gro o(D; 5 @ .to 11-:>:ro (- ö.L ã< c d-o t-- p. Fl Ffi (t, .f (! o ,ñ(n o<^ o i.õv z -!€oFñÞofr¡ \¡/J. H (- o , r-tø F.F¡¿ { o J:tooõ ^H. m I o Þrc J = I !fvõlÍl I O -. O É EÞ @ ) 5E O 5 f\) (- I-FJ È F-Þ rt ->¿ J J F-^ cfo Er ø tt^(0 J v v¿ O Fñ z . r+Ép.rn¡J U¡ 5ìJ r'' O t-rt ãõop' -l IC P.J J HE d.'Q / oo(0 D g¡ rñH.JP. CT J r-.õ J NÉ II- O F'Ëìl< @ tft r+ Hlür C.) o lt-' C- / < /¡Élo -o 0 H ò8Id ta ä'J^ o o. I oti g? ctl O.L a Page 106 I 60 FLOWERS l-z40 J o- É, l¡¡ o- ctz z õ20 I \ R|PE FRU|T = ^ I ^ I \ I \ ./ I o - +- a -+€- M A M J A o N D I M A M J A s o N o î M A M I 8t 82 83 TIME Fig. 4.21. Hean no. of flowers (--*-) and ripe fruit ç-O-) per plant of Lvsiane exocarpÍ along the 3.3 km traverse. Sample sizes varied between 67 - 78 plants. JFMAMJJASOND JFMAMJJASOND I .-.- 80 b-- Heterodendrum 8l --õ- Exqcarpes oleaelolium a2 anhyllrJs lruits 83 frults I ¡ 80 Enchylaçna My¡noruo 81 þne0tes piaty¡arum 82 .-3- fruits flowers I 83 -- t ¡ + 81 Rhagodla Chenopo¡liuo a2 sR¡oeÂce¡s oaudichaudianum 83 lrults -- 1 --- frults JFMAMJJASOND JFMAMJJASOND Fig. 4.22. Fruiting and flowering seasons of six perennial snecies in the study area. Àrrows indicate the beginning and end of observations. Broken Iinel signify datelines, and do not impty incidence of floç¡ers or fniits. ÇHÀPJEB-5 THE ECOLOGY OF THE SPINY-CHEEKED HONEYEÀTER ÀND HISTLETOEBIRD 5.1 INTRODUCTION Birds which feed on the floral nectar and fruit of mistletoes vary in their dependence on the plants as a food resource. The white-cheeked cotinga is a specialised mistletoe-feeding frugivore and is dependent on individual species of mistletoe in various parts of the Peruvian Àndes (Parker 1981). The mistletoes fruit continuously, so one might surmise that Iocal populations of the cotinga are obligately dependent on the particular mistletoe at a site. However, most bird-mistletoe mutualisms are less specific than this, and even specialised mistletoe-feeding birds tend to utilise a guild of plants in the one area (Liddy t982a, 1983; Godschalk 1983b; Davidar 1983a). The aim of the work reporbed in this chapter was to ascertain which birds consumed the fruit of Àmyeme quandang in the study area, and to determine their degree of ecological dependence on the mistletoe population. The spiny-cheeked honeyeater and mistletoebird were found to be the most important consumers of fruit (both species) and floral nectar (spiny-cheeked honeyeater). For each species, I asked the foll.owing questions. tJhat importance dÍd f,- E¡andgng nectar and fruit have in the overall diet; to what extent were fluctuations in population density explicable in terms of mistletoe flower and fruÍt abundance; did the fruit and nectar resource influence territorial systems or spacing in the population, and the timing and intensity of breeding? Page 108 5,2 HETHODS 5.2.1 Birds eating mistletoe fruit I watched birds feeding in mistletoe canopies whenever opporbunities arose during fieldwork and recorded those which fed on fruit. I mistnetted birds in the trapping area in December 1980 and bimonthly between November 1981 and November 1982 and collected their faeces to determine which species were eating mistletoe fruit. Faecal samples were obtained by one of two methods (Ford e! eL 7982). Prior to January 7982, I wrapped birds in absorbant paper envelopes and secured them in paper bags. Àfter 30-110 min the birds were removed and any excreta adhering to the plumage transferred to the paper envelopes. Envelopes srere labelled and dried. Later in the Iaboratory, paper discs containing the faeces were cut from the envelope, placed in a petri dish containing 70% ethanol, and the egesta scraped from the paper. The second method, used between January and November 7982, involved the confinement of birds in 2 I plastic containers provided with small holes in the lid for air and a raised bottom of wire netting (1 cm mesh). Larger birds such as spiny-cheeked honeyeaters were left in containers for 30-180 min and smaller birds the size of mistletoebirds were kept for 45-110 min, depending on the time since last capture, weather conditions and time of day. The faeces at the bottom of the container were mixed wibh 70% ethanol and transferred to a labelled glass via]. In the laboratory faecal samples were immersed in 707. ethanol in petri dishes and examined under a dÍssecting microscope. The number of mistletoe seeds were scored. For spiny-cheeked honeyeater and mistletoebird sampl.es, the solid fractions in each sample were identÍfied and their percent contribution to the total volume of solids in the sample estimated to the nearest 5% (Rowley & Vestjens 1973). 5,2.2 Bird census I censused birds along the 3.3 km traverse in the study area on 38 Page 109 occasions between Àugust 1980 - July 1983. I used a relative index transect method (Shields 1979), and counted all individuals up to 50 m on either side of the traverse. The 33 ha census area eras staked at 100 m intervals with painted posts, and surveyors' tape of different colours was tied to trees and shrubs in order to delimit the boundaries. I walked at a rate of 25 m min{ on a variable course depending on where birds were concentrated. Àll individuals which flew over or perched in the census area were counted, irrespective of their distance from the observer. Censuses began about 30-40 min after sunrise, Iasted 132 min, and were only conducted on still, relatively cLoudless mornings. I averaged 1 census mo{ but, at times, conducted two or three in close succession to examine the short-term variation in counts. Census results for the entire bird community are shown in Appendíx 2, 5,2,3 Spiny-cheeked honeyeater and mistletoebird diets The diets of the spÍny-cheeked honeyeater and mistletoebird were determined from foraging observations (Hartley 1953; Ford & Paton 1977: Thomas 1980), time budgets (Paton 7982a), and the examination of faeces (Ford e! ef, 1982). I recorded foraging observations during frequent periods of fieldwork between June 1980 - October 1983. I searched widely for foraging birds in the study area at all times of the day, and attempted to guard against observational biases. For instance, birds in dense western myall and Àmyema ggandaDg canopies L¡ere less conspicuous than those perched on dead trees or in flight; vocal individuals were more easily detected than silent ones. I scored up to 10 consecutive foraging actions (defined as attempts to procure or reveal food with the biII) every 5 min per individual. The data for one individual in a given 5 min period was termed a foraging observation. In recording foraging actions, I noted the following details: bird species, food item, height above grround (ground, bush, shrub or tree, above the tree canopy), substrate foraged on (foliage, branch, Page 110 litter), plant species (where relevant) and foraging behaviour, defined in Table 5.1 . Bimonthly, between November 1981 and December 1982, I time-budgeted birds encountered during searches of the study area. I timed individuals' activities for as long as possibJ.e. tlhen I lost sight of a bírd I attempted to regain contact and continue the time budget. ÀctivÍties were timed with a digital wrist-watch to the nearest second. Foraging rates were sirnultaneously measured with a stop-watch. Spiny-cheeked honeyeaters were time-budgeted for a total of. 22 hr. They were generally wary and difficult to follow at a distance close enough to record their activities continuously. The difficulty ç,as exacerbated by the density of western myall and Amyema quandang canopies. The average lengbh of time for ç¡hich continuous contact was maintained was 125 s. I collected 15 hr of mistletoebird time budgets. The ease with which the time budgets were obtained varied seasonally. The longest spans of data were collected between l.farch and JuIy when birds sometimes sat in the one canopy for tens of minutes. Contact was difficult to maintain between October and January when birds frequently moved between trees and traversed large areas rapidly. Contact was maintained with individuals for an average of 203 s. Long periods (> 10 min) of unínterrupted data ç¡ere obtained in each month. Corroborative evidence of diet was obtained from the examination of faecal samples from mistnetted birds (section 5,2.7). I also noted aII defaecations while observing or time-budgeting birds, ard usually collected the excrement. Faeces of the spiny-cheeked honeyeater which contained a ).arge volume of insect or plant matter were easier to find and collect, due to their bulk, than small or fluid samples. Accordingly, the egesta collected in the field were biased towards bulky samples of solids. Field samples were immediately placed in labelled petri dishes ard notes made on their macroscopic composition. Samples were exarnined in the Laboratory as described in section 5.2.1 . Page 111 5.2.4 Territoriality and behaviour Some spiny-cheeked honeyeaters and mistl.etoebirds were individually colour-banded and studied intensively in the fieId. Honeyeater territories were mapped in the trapping area by two observers over a 3 d period in June 7982. Individual birds and pairs r¡ere followed, and the positions where they sang, foraged at food plants, and interacted with neighbouríng birds were marked on xeroxed copies of an aerial photograph of the area. The recording of the birds' positions was facilitated by the 100 m x 100 m grid (Fig. 2.2) . I made notes on the behaviour and breeding of spiny-cheeked honeyeaters and mistletoebirds throughout the study. The most intense period of observations was between November 1981 and December 7982. 5.3 RESULTS 5.3.1 Birds eating mistletoe fruit 0i the 19 bird species mistnetted between December 1980 and November 7982, only the faecal samples of the spiny-cheeked honeyeater and mistletoebird contained mistletoe seeds (Table 5.2). In addition to these species, seed-predating parrots (section 7.7.3.3) t¡ere observed eating mistletoe fruit and at least three other species probably ate fruit in the study area. Rebecca $loodell (pers. comm. ) observed a red wattlebird Ànthochaera camnculata probing Àmygma quandang flowers and consuming fn¡it in a nearby paddock in October 1983. In Àprit 1983, Àustralian ravens Corvus coronoideg and little crows Ç^ bennetti congregated at kangaroo carcasses near the trapping area over several days. The ground and low perches rounda.bout were splashed with con¿id droppings. Àmongst the egesta were clumps of Heterodendrum cleeefolium seeds and 1 to a feç¡ Àmvemq quandanq seeds. About 30% of the mistletoe seeds had germinated. Emu Dromaiug novashollendtee dung often consisted entirely of the Page 112 developing and ripe fruits of Àmyema o,uandeg in summer. In winter, dung sometimes contained a few fruits of Lysiane exocarci, and graze lines were occasionally evÍdent on fruiting mistletoe canopies where bÍrds had removed all the ripe fruit below about 2,7 n. Some !- gxecslpl seeds germinated after passage through emus, but not À- ggandanq seeds. 5.3.2 The spiny-cheeked honeyeater 5.3.2.1 Diet The main components of the diet of the spiny-cheeked honeyeater as determined by foraging observations were nectar, insects and fruit (Table 5.3). The floral nectar of Àmyems qugndanq dominated the diet in winter and spring, and insects and A- quandenq fruit comprised the main components in summer and autumn (Fig. 5.1). Ílhen feeding on the ripe fruits, birds pecked the middle of the fruit to remove the distal half of the epicarp, ard consumed the protruding fteshy seed*, leaving the basal hemisphere of the epicarp attached to the plant. Birds frequently pecked frr.¡its r¿hich were not fully ripe several times before splitting the epi.carp. Various other food plants were of lesser importance (Table 5.4), notably the floral nectar of tysiana exocarni in late summer and the fruits of various shrubs and bushes. The small succulent leaves of Lvcium australe were eaten throughout the year but mostly in late surnmer. Honeydew, secreted by phytophagous eurymelid bugs, sras consumed on cool mornings in summer, when attendant ants ç¡ere unable to harvesb all the secretions. Spiny-cheeked honeyeaters mainly foraged for insects at tree height, but also spent time searching among the bushes, on the ground or sallyir¡g above the tree canopies (Table 5.5). Sallying was the main foraging behaviour employed, although gleaning from foliage and branches was also important (Table 5.6). The behaviour of spiny-cheeked honeyeaters when *The diaspore or dispersal unit in Àmvgma quandang ard Lvsiqna exocaroi is_ generally referred tó as a seed, and comprises the true seed, erdocarp, ard án adheränt viscid mesocarp which is partly removed dr:ring digestion by frurgivores (see section 7.1,3.1). The diaspores of both plants are referred to as 'geeds' hereafter. Page 113 foraging for insects was influenced by rain, particularly in summer. Fiying insects were abundant during the afternoons for a number of days after rain, and birds capitalised on such conditions in November 1981 and }larch 7982, spending large amounts of time sallying from exposed perches. tlhen flying insects were not abundant, more time was spent searching for insects in tree and shrub canopies and in the bush stratum, and gleaning, saì.Iying and snatching techniques $rere used more evenly. The time çrhich honeyeaters spent foraging for different food items in 1981-82 is shown in Figure 5.2. Foraging actions tallied in the sane period are shorìn for comparison. The two methods provided broadly similar results: insects and Amyema ouandanq fruit were important food items in November 1981 and January 1982, foraging for insects predominated in March, and f cruandang nectar was sought mainly thereafter. However, consistent differences between time budgets and foraging observations were evident. (1) The amount of time which birds spent foraging in tree canopies and bushes was usually a greater fraction of foraging time than the corresponding proportion of foraging actions. (2) The fraction of foraging time spent in ftight, hawklng lnsects away from vegetation, was usually several times smaller than the corresponding proportion of foraging actions. The difference in diet betv¡een November 1981 and November 1982 was marked. l{hereas insects and Amyemq quandang fruit domínated feeding in 1981, mistletoe nectar was sought primarily in 7982. The difference was related to the effect of the drought on mistletoe reproductive phenology. In November !987, most large plants had finished flowering and had begun to mature the new season's fruit. Midway through the month the standing crop of fruit was virtually nil, but the large numbers of epicarp bases on plants indicated that birds were harvesting the fruit as it ripened. À sr-rnrey of 280 plants at the end of the month showed that most large plants bore a few semi-ripe fruit, and that the rate of fruit maturation had exceeded the birds' ability to harvest it. In November 7982, many plants were still in tight or moderate Page 114 flower and the last few fruit of the previous year's crop were being ripened. The bimonthly time budgets of spiny-cheeked honeyeaters between November 1981 and October 1982 are shown in Table 5.7. Foraging time constituted 29-542 of birds' day-time activities. In winter, birds visited an average of. 7778 flowers day{ (pooling data between Hay and 0ctober), and made 143 foraging actions day{ for insects. In summer, foraging for insects increased Lo 329 foraging actions day'. Similar amounts of time were spent foraging for Àmvema suandang fruit in November 1981 and January 7982, but estimated consumption was 315 seeds daya Ín January compared to 101 seeds day{ in November. In March, little fruÍt $ras consumed and the bulk of the diet consisted of insects. 5.3.2.2 Faeces The soLid fraction of faecal samples obtained from mistnetted spiny-cheeked honeyeaters was composed mainly of fruits and seeds, insect remains and uric acid (Fig. 5.3). In the summer months, Amvema cruandanq seeds dominated the faecal material, the largest individual sample containing 25 seeds. Insect remains and the fruits and seeds of other plants ç¡ere also well represented. The volume of solids in the egesta greatly diminished in winter, concommitant with an increase in clear fluid which was presumably digested nectar. The smaLl fraction of soLíds in May and JuIy 1982 consisted mainly of insect remains, uric acid and plant material other than místletoe seeds. The range of items defaecated by honeyeaters (Table 5.8) closely matched field observations of their diet (Table 5,4). Histletoe seeds, insect remains, the seeds of Rhggodiq spinescens, Enchvlaena tomentosa and Exocarpcg epÞyliug, and LvciUn eugtrale leaves were the most frequent items found in the solid fraction of the faeces. In accord with the seasonal fruit production of most of the plants, the occurence of various fruits and seeds Page 115 in the faeces r¡as seasonal. From the plant viewpoint, spiny-cheeked honeyeaters egested and dispersed large numbers of seeds of most of their food plants. Faecal samples of birds trapped at four other locaLitÍes on Middleback in 1980-81 (Table 5.9) provided additional information on spiny-cheeked honeyeater diets. In October 1980, large nunbers of birds, many of them juveniles, visited fruiting peppertrees gchinug areiqg at the Middleback shearers' guarters. The seeds and shells of peppertree fruits and, to a lesser extent, insects contributed the bulk of the faecal samples. In February 1981, a high density of flowering Lvsiana exocarpi and fruiting Heterodendrum oleaefolium attracted birds to part of the study area in mid western overland paddock. The solid fraction of the egesta of four birds caught in mid morning was dominated by a few seeds and arils of U- oleaefolirlm. Surprj.singly, none of the stools contained f ggqndanq seeds. H- qleaefolium produced few fruit in 1982 and 1983 (Fig. 4,2?), accounting for the paucity of foraging observations on the fruit and the lack of seeds or arils in faecal samples (Tables 5.4 & 5.8). 5. 3. 2.3 Population dynamics The abundance of spiny-cheeked honeyeaters showed a cyclical trend, with high numbers between autumn and spríng and low numbers in early summer (Fiq. 5.4). Superimposed on the seasonal pattern sras a tendency for lower counts as the study progressed. À multiple regression analysis, incorporating time and two cyclic functions with a 12 mo period as the independent variables, proved highly signifícant, explaining 55'/, of the variation in counts (Table 5.10). Each partial regression coefficient was highly significant, indicating that both the annual cycle and long-term trend in spiny-cheek numbers were important sources of expJ.ained variation. À multiple regression analysis employing Àmvems quandanq and Lvsieng eËgcarpi fruit and flower abundance as the independent variabLes failed to Page 116 demonstrate the importance of most of the plant variables in contributing to the variation in spiny-cheeked honeyeater counts. Only À- quandanq flower aburdance had a significant partial regression coefficient (Table 5.10). The linear regression of spiny-cheek counts on À^ SJgDdgnq flowers, although significant, was not a useful model because the relationship between the variables was hyperbolic (Fig. 5.5): the number of birds tended to asymptote at relatively Iow flower abundances. 5.3.2.4 Breeding The timing, duration and intensity of breeding in spiny-cheeked honeyeaters differed markedly between years (Fig. 5.6). In the latter half of 1980 and in 1981 and 7982, egg-laying was confined to Àugust-September. In 1983, egg-laying occurred in at least April, l'lay, July, August and gctober, and four pairs which I watched over several months all built at least two nests and reared at least one brood to nestling stage. Two col.our-banded females (Bu/t{ and 0/0) Iaid two and three clutches of eggs respectively. The intensity of breeding differed greatly between 1982 and 1983. In 7982, most of the 16 pairs under observation made little or no attempt to breed. Two colour-banded females showed interest in possible nesting material on single occasions in JuIy and Àugust. Two further pa.irs had buílt nests by mid Àugust which then went unused. Only one pair reared young, probably laying in early September. Sightings of two independent juveniì.es in gctober ü¡ere the only, indication that other birds in the general area bred successfully. I spent less time in the field in 1983 and proportionately Less time observing spiny-cheeks. However, I repeatedly stumbled on evidence of breeding in the course of various activities. 5.3.2.5 Pair bond Spiny-cheeked honeyeaters which were resident in the study area generally occurred in pairs, especially when food was localIy sufficient to Page 117 maintain a moderate to high density of birds. Paired birds naintained freguent contact during the day, and foraged and rested together. Some pair bonds were maintained over many months. Five pairs of colour-banded birds were observed together for a minimum of 2, 6, 7, 10 and 16 mo during 1982-83. Two pairs were still intact at the end of the study after 10 and 16 mo. I assumed the remaining three broke up when one or both partners disappeared and were not recorded again. In no known instance did an individual leave its partner and pair with another r.rhile the former mate remained in the area. 5.3.2.6 Site fidelity and territoriality Spiny-cheeked honeyeaters in the study area were mostly sedentary. Two-thirds of 33 birds which I mistnetted between December 1980 - November 1982 were retrapped or observed one or more months after first capture. 0n the basis of observations and trapping records, they remained in the area for an average of 15.5 mo (range, t-27 mo). At least half were still present at the end of the study in late 1983 or early 1984. Fourteen birds showed a marked degree of site fidelity, and were repeatedly observed or trapped in the same few hectares and net sites over many months. The best example concerns the pair, Bu/t'l and 0/Il. I observed them for ?7 and 24 mo, respectiveì.y, during which time they remained faithful to a territory of about 7.5-2.5 ha (Fig. 5.7). Six birds also showed strong site attachment to particular parts of the trapping area, but changed territories partway through the study The territorial behaviour of birds varied seasonally. Pairs spent most or all of the time on their territories between late March and September 1982, initÍally feeding on insects and fruits of místletoe and other plants, and switching to ÀmvgBg quandanq nectar as flowers becane more abundant. Territories were defended by both sexes: birds sang throughout much of the day, and challenged or chased intruding conspecifics as well as Page 118 other species. The position of 16 honeyeater territories mapped in June 1982 is shown in Figure 5.9. Figure 5.8 displays the field data for the five pairs which contained at least one colour-banded bird, and for a sÍxth individually identifiable bird with an abnormal tuft of feathers on the abdomen ('Tuft'). The boundaries between adjacent territories were sharply demarcated (Fig. 5.9), because birds tended not to intrude on their neighbours' territories. Despite shepherding attempts, pairs were reluctant to be pushed in one direction for very far and soon double-backed past the observer to areas from which they had just come. Territory size varied betç¡een 1-5 ha. The smallest territories in the southern part of the trapping area supported the largest biomass of Amvema quandang. Àlmost the entire gridded portion of the trapping area $ras visited by spiny-cheeks over the 3 d, and r¡as deemed to be occupied by one or other pair. The few parts not visited by spiny-cheeks had low tree densities (cf. Figs 5.9 e 5.10) and supported little or no mistletoe. Pairs were no longer present on their territories continuously by late October 1982. For the subsequent 4 mo, at the height of the drought, spiny-cheeked honeyeaters $rere usually difficult to find in the area. Birds foraged widely for food during the period, but occasionally visited their former territories and adjacent areas and searched the mistletoe canopies for fruit. After visiting the trapping area, birds usually flew up and off in various directions and were lost in flight several hundred metres anay. I found 0/t{ amongst a congregation of spiny-cheeked honeyeaters feedirrg at Eucalvptus torouate flowers at the homestead, 4 km south of the trapping area, in November. During a heatwave in Febnrary, 10 colour-banded birds drank at the water trough 1 km south of the trapping area durir¡g 5 hr of observation. Males remained reasonably close to the study area, although spending Iittle time on their territories. During showers of rain one afternoon in February, three colot¡r-banded males appeared on their former Page 119 territories, hawking flying ants from exposed perches and singing intermittently. Females were less often recorded in the trapping area and were outnumbered, 4 to 1, amongst the colour-banded bÍrds at the trough. After the rains in Harch 1983, the behaviour of spiny-cheeked honeyeaters reverted dramatically. In late March, pairs and individuals were continuously distributed through the wooded areas and birds sang repeatedly. Territorial behaviour was maintained in ApriI when breeding commmenced (section 5.3.2.4), and continued untiL October. Territorial birds initially fed on insects and fruÍts after the drought, mistletoe nectar not becoming available until winter. 0bservations early in the study indicated that the behaviour of spiny-cheeked honeyeaters in the summer of 1982-83 was atypical. Unfortunetely no individuals were colour-banded in the earlier summers, Bo the details are unknown. However, birds were continuously present in the study area in both the 1980-81 and 1981-82 summers and tended to occur in pairs, individuals defended fruiting mistletoes by the repeated displacement of intruders from trees, males engaged in territorial singing contests, and birds sang frequently. These observations suggest that spiny-cheeked honeyeaters held territories in pairs across both summers in much the same way as they did between autumn and spring in 7982 and 1983. 5.3.3 The mistletoebird 5.3.3,1 Diet The fruits of Àmvemq crugndanq dominated the mistletoebird's diet throughout the year, accounting for at least 75% of. foraging actions (Fig. 5.11). Insects formed 70-20% of the diet, and À, quendang nectar and Lysiana exocarpi fruit were consumed in small amounts in winter and spring. I saw one bird take an Exocarpos aphyllUg fruit, the only record of a non-mistletoe fruit being eaten in the study area. Mistletoebirds handled Àmveme quandanq fruits in the same çray as Page 120 spiny-cheeked honeyeaters. They split the rind to remove the distal hemisphere of the epicarp, and extracted the seed, leaving the basal half of the epicarp attached to the plant. Unripe fruit were freguently tested with a peck to see if the epicarp would split, and semi-ripe fruit often regrrired more than one peck to remove the distal portion of the epicarp, or to remove the seed. Lvsiana exocarni fruits were handled differently, due to the skin-Iike epicarp. lJhereas spiny-cheeked honeyeaters plucked and ingested individual fruits entire, mistletoebirds retired with a fruit to a perch just beyond the mistletoe canopy. The fruit was juggled in the bill and the mandibles inserted inside the skin through the hole left by the fruit stalk. The seed was swallowed but the bird continued to'r.,ork'the skin, sucking out the fleshy mesocarp and eventually dropping the evacuated epicarp. The handling time for individual fruits was long, averaging 42 s (range 74-71 s) between the time the fruit was picked and the skin discarded. l,lhen foraging for insects, birds searched the branches and foliage of trees and shrubs in a series of hops and short flips. Occasionally, individuals hovered near a substrate for several seconds and inspected it for food items. llhen searching canopies, mistletoebirds usually flicked both wings out from the body in a flycatcher-Iike manner, presumably in order to flush resting insects. The average rate of wing-flicking while foraging for insects was in the range 7-18 wing flicks minr (Table 5.11). Mistletoebirds mostly gleaned branches for insects, although snatches and sålIies inside canopies comprised 35% of foraging actions (Table 5.12). Birds were often successful in capturing prey, judging by mandibulations. 0ccasionally an insect or spider was visible in a bird's bill, or the flying insect which a sallying bird chased was seen by the observer. The arthropods which were consumed ranged from very small in size to moths, 1.0-1.5 cm long. Figrure 5.12 shows the proportion of time spent foraging for different food items, compared with foraging actions tallied dtring the same Page 12t periods. Foraging for Àmyema cnrandqnq fruit constituted more than 70% of mistletoebird foragÍng time in aIl months except March, when approximately equal time was spent searching for insects and fruit. Foraging for insects accounted for less than 30% of foraging time in other months. Foraging observations consistently overestimated the proportion of foragÍng time spent searching for fruit. Likewise they underestimated the amount of time spent insect foraging. The differences were related to the rates at which mistletoebirds made foraging attempts when feeding on insects and fruit. 0n average, birds made over three times as many foraging attempts (pecks) when searching for fruit as they did çrhen foraging for Ínsects (Table 5.11). Foraging time constituted 22-36% of mistletoebird activÍties (Table 5.11). Large numbers of fruit çrere consumed throughout the year, peaking in winter at 256 Ànyema suandanq and 24 Lvsiana exocarpi seeds day{ (data pooJ.ed for May and July). Fruit consumption declined to 177 cn¡andanq ^- seeds day{ in November 1981 and September-October 1982 (data pooled). Mistletoebirds made 69 foraging attempts day{ for insects (all data pooled), The amount of foraging for insects varied between months but not in a detectable seasonal pattern. The sample sizes of obsen¡ations in some months were small so the monthly values were proba-bly subject to large errors. 5 .3.3.2 Faeces Faecal samples were obtained from 72 of. 13 mistletoebirds netted in the study area between 1980-82. Àtl samples consisted simply of mistletoe seeds, mainly those of Àmyemg quandang. Two contained Lvsiênq exocarpi seeds. Microscopic examination revealed traces of insect exoskeleton in one sample. The stools of mistletoebirds $rere readily found by watchirg birds defaecate, because of the bulk of the seeds therein ard the habit of depositing the faeces on the perch (section 7.4,3.1). t'listletoe seeds were Page L22 contained in 962 of the samples (Table 5.13). The remainder consisted of uric acid, or a smaLl amount of viscin from mistletoe seeds, or both. Àmvema quandang seeds dominated mistletoebird excreta throughout the year. There was little seasonal variation in the number of seeds defaecated per stool, averaging 2,6 !.17 (78Ð overaLl. One or tr¡o tySiêna exgcarpi seeds occurred in nine stools between Hay and JuIy, and were usually passed in the absence of À^ quandanq seeds. Urates $,ere passed with or without mistletoe seeds at all times of the year, and traces or more substantial quantities, sometimes coating most of a seed, were found ín 63% of samples. Macroscopic remains of arthropods were found in only two stools in September 7982. Microscopic examination of grey stains on two seed strings in July and September also revealed traces of exoskeleton. However most mistletoebird stools which were collected in the field and examined microscopically were founcl not to contain invertebrate exoskeleton. Birds mistnetted at the shearers' quarters in October 1980 defaecated mostly peppertree berries and epicarp fragrments. One bird in I'langa paddock, 15 km south-east of Hiddleback homestead, defaecated two Amygma miraculosum seeds in Myoporum platvcarpum open-woodland infested with the mistletoe in ÀpriI 1981. 5.3.3.3 Population dynamics Histletoebirds were recorded in 87"¿ of. censuses (Àppendix 2). Counts were generally low (Fig. 5.4), averaging 2.8 birds censusr. Two temporal trends in abundance proved to be significant (Table 5.10). Counts declined over the 3 yr period suggesting a reduction in population density due to the drought. Numbers also displayed a weak annual cycle ç¡ith lowest counts generally in March-AprÍl and high counts at various times between May ard February (Fig. 5.4). These two periods comesponded with the non-territorial and territorial phases in male behaviour, respectively (section 5.3.3.4). Page 123 Hence the annual pattern in counts may have reflected seasonal changes in mistletoebirct detectabil ity rather than f luctuating population density. Regressions of mistletoebird counts on Amvema E¡andang and Lvsianq exocarpi fruit abundance were not significant. Evidently, the size of the standing crop of fruit did not strongly influence mistletoebird abundance which appeared to remain fairly stable most of the time (Fig. 5.4). The absence of a relationship between fruit and mistletoebird abundance was best exemplified in late Harch 1983, after the drought. The standing crop of L- quandeng fruit was about as large as at any stage during the study (Fig. 4.2), but birds !¡ere more scarce than at any other time. 5 .3.3. 4 Breeding Several nests were found in the summer of 1980-81 (Fig. 5.13) when the territorial behaviour of five pairs along the traverse was intense and their breeding behaviour conspicuous. 0nly two active nests were found in subsequent seasons. The lack of breeding evidence in 1982-83 was due to a reduction in the amount of breeding, because most time was spent observing birds in this period. Breeding was recorded over several months in different seasons (Fig. 5.13). Egg-Iaying occurred between JuIy and September in 7981,1982 and 1983, and between November and January in the summers of 1980-81 and 798I-82. No evidence of clutches begun in October was obtained. The spring and mid summer peaks in breeding occurred either side of the annual decline in the abundance of Àmvema quandang fruit between October-November. Mid summer breeding occurred in those seasons when fnrit was abundant but not in t982-83 when fruit was scarce. Spring egg-layirg occurred in 1981 when the standing crop $ras low and declining, in 1982 when there was a moderate amount of fruit available, and in 1983 when fruit was plentiful. 5.3.3.5 Site fidelity Limited information was obtained about mistletoebird site fidelity Page 124 and territoriality because few birds were caught and banded, and sedentary individuals occupied large home-ranges or territories () t2-25 ha). Fourteen birds were mistnetted in the study area between December 1980 and September 7982. Host did not remain for more than a few days or weeks after banding, judging from observations of banded and unbanded birds. One colour-banded male remained faithful to a territory of about 400 m Ín diameter for 11 mo and nested there. At least one other male occurred in the area in which it was trapped for at least 9 mo after banding. Other males freguented parts of the study area for up to 3 mo between JuIy and February. One female bred near the area she was trapped in, 12 mo after banding, but whether she remained in the area in the intervening period is unknown. The banding evidence is equivocal as to whether other females remained in the study area for longer than the period required to breed. t{hile some individuals were resident for 6 mo or more, most appeared to remain in the area for periods of a few days to 3-4 mo. 5.3.3.6 Behaviour Ìlistletoebirds usually occurred alone or in pairs. In autumn and winter, individuals often spent periods of an hour or more without moving more than a few metres in the one grove of trees. They interspersed foraging bouts in mistletoes or adjacent tree canopies with preening and resting periods lasting up to 10 min. À resting period ç¡as usually terminated with wing and leg stretching, defaecation and then a return to foraging, or fI ight. Courtship behaviour was seen as early as April and as late as February, but was concentrated between Ìlay and September, and coincided with an increase in territorial behaviour in males. Territorial males were hyperactive, darting between various parts of the territory and singÍng from exposed perches. Neighbouring males chased each other in protracted high speed weaving flights above territory boundaries. HaIes maintained Page 125 their restless behaviour and territorial singing until January or February. 5.4 DISCUSSION 5.4.1 Birds and mistletoe fruit The spiny-cheeked honeyeater was the most abundant species in the study area (Àppendix 2) and individuals consumed large numbers of Àmyems E¡andanq seeds per day in the summer months. The density of mistletoebirds was low but birds occured in the study area throughout the year and individuals consumed large numbers of seeds per day both in summer and winter. The red wattlebird, Iittle crow and Àustralian raven occurred in low densities and only the latter was resident in the study area (Appendix 2). Red wattlebirds foraged at mistletoe flowers in the study area and were rare in summer when nectar çras unavailable and fruit most abundant. I did not observe corvids foraging in the study area due to their wariness. Hovtever, observations elsewhere on the station indicated that they were omnivorous. Considering their low densities and the minor component of fruit in the diet, corvids and red wattlebirds must have consumed negligible quantities of À- cruandanq seeds in comparison to the spiny-cheeked honeyeater and mistletoebird. Emus were seed predators of Amvemg úuandanq because the seeds were killed by passage through the digestive tract. Emus were ineffective dispersers of lvsiane exocarpi seeds, some of which germinated in the dung, because birds defaecated on to the ground. Presumably the only possibility of emus effectively dispersing mÍstletoe seeds would be for a bird to defaecate on a seedling or young plant of a compatible host species. The chances of this seem remote. The predominance of mistletoe fruit in the diets of only two frugivorous birds was noteç¡orthy in a community containing several partial or opportunistic fn:givores. The singing honeyeater Lichenostomus virescens Page t26 Q6 g) frequently ate the fruits of lncþvlcens tomentosa, Rheqedia spincscens, Chenopodium qaud-tgþqgdiqnum and lxocarpqg aphvllus, but did not 'a attempt to harvest [myema gganda¡g or lysiane execeroi seeds. This is surprising because there are several records of mistletoe seeds in the digestive tract of the species or of birds feeding on mistletoe fruit (Reid 1985). Singing honeyeaters !¡ere unlikely to have been aggressively excluded from mistletoe fruit by the larger spiny-cheeked honeyeater because they s¡ere persistent floral foragers at Àmvemg suandanq despite repeated dÍsplacement from flowers by the larger species. I suspect that the seeds of both mistletoes were too large for singing honeyeaters to feed on. Spiny-cheeked honeyeaters took a long time to pass f quandang seed strings (section 7.4,3.1) and the identified mistletoes on which the singing honeyeater has been reported to feed have smaller fruit than f,- quandgng. I once watched a singing honeyeater peck a berry of the small fruited !- murgayi. The bird did not attempt to ingest the fruÍt but placecl it on a branch and pecked at the succulent mesocarp. These observations suggest that À- E¡andanq seeds are too large for singing honeyeaters to swallow or pass. Black-faced Artamus melanops, dusky !- cinereus and masked woodswalLows |- personatus, grey butcherbirds Cracticus torsuatus, Àustralian magpies Gvmnorhinq tibicen and grrey shrike-thrushes ColluricÍncla harmo¡igg occasional.ly ate Exocarpos aphvllus fruit but were not recorded taking mistletoe fruit. The seeds of Amyema quandanq are unlikely to have a lor.¡ nutritional value because spiny-cheeked honeyeaters and mistletoebÍrds were dependent on the fruit seasonally or throughout the year. I suspect that large viscid mistletoe seeds are difficult for small to medium sized opportunistic frugivores to handle or pass, and that the larger opportunÍsts such as corvÍds and magpies may generally be deterred by the difficulty of foraging in dense thin-stemmed canopies. Page 727 5.4,2 Comparison of foraging observations and time budgets to elucidate diet Paton (1982a) guestioned the value of feeding obsenrations in elucidating the diets of honeyeaters because observations of birds made by an observer walking through an area tend to be biased toç¡ards individuals performing conspicuous activities. The bias is avoided when a statÍonary observer spends long periods time-budgeting the activities of a temitorial bircl which does not move out of range or sight. l'fethods involving the scoring of foraging observations have advantages in utility and efficiency over time-budgeting. Foraging observations can be scored quickly during short bouts of fieldwork. Time-budgeting reguires the observer to spend long periods in the field devoted entirely to one activity. The advantages of time budgets are that they estÍmate the daily consumption of food items, and coupled with biochemical data, yield information on the nutritional value of dietary components (Paton 7982a). The compromise adopted in this study was to collect both sorts of data. Foraging attempts were scored throughout the study and time budgets lrere measured over a 13-14 mo period. Comparisons of the amount of fruit, insects and nectar in the diets of spiny-cheeked honeyeaters and mistletoebirds as deduced from foraging observations and time budgets are shown in Tables 5.3 and 5.14. The foraging observations did not estimate per cent foraging time Deg se because I recorded up to ten foraging actions per observation rather than one, but there $ras reasonable agneement betç¡een the two techniques nonetheless. Foraging observations terded to overestimate the proportions of time spent feeding in categories in which the rate of foraging actions $ras highest, such as nectar or fruit feeding, and underestimated the foraging time for foods which were harvested slowly, such as insects. Time budgets collected by a mobile observer following errant birds which are freguently lost to sight are theoretically subject to the same biases of detectability as foraging observations (Hartley 1953; Paton 1.982a) and avian census techniques (Shields 7979). The faecal samples from Page 128 spiny-cheeked honeyeaters indicated that similar quantities of mistletoe seeds and insects were defaecated in November and January (Table 5.15), but the time budgets suggested a three-fold increase in the consumption of seeds in January. The two data sets also differed in estimates for the reduction in seed consumption in Harch. The most probable explanation for the discrepancies was that the time budgets were biased towards conspicuous foraging behaviour such as hawking insects in November and March and foraging for insects amongst the bushes in November, at the expense of inconspicuous foraging behaviour in tree and mistletoe canopies. Faecal samples obtained from mistnetted birds or by watching defaecating birds were not subject to sampJ.ing bias towards particuLar foods in different months, because samples r¿ere obtained throughout the day (Table 5.15) and over most of the trapping area in each month. The estimate of seed consumption in March was also subject to large error because of the small sample of observations in that month (Table 5.7). Recent developments in avian census techniques which strive to rneasure bird densities rather than relative abundance (Shields 7979) suggest one solution to the problem of detectability biases when recording foraging data. If the distance to the bird was estÍmated ç¡hen foraging data were recorded, the data could be analysed to determine whether the freguency of foraging in various categories varied dÍfferentially with increasing distance from the observer, a situation which would denote bias. Às in the census technigue advocated by Shields 1979), distance intervals could be specified for each foraging activity in which detectability biases appeared to be least important. 5. 4.3 Spiny-cheeked honeyeater 5.4.3.1 Diet Host of the foods which spiny-cheeked honeyeaters ate at Hiddleback have been reported previously, g-SL the fruits of Heterodendrum oleaefolium, Page 129 Lycium sp., Enchy-Lae¡e tomentosa, Rhegodia spp, and the peppertree (Sutton 19261 Pearse 1929; Lea & Gray 1936; Coleman 1938; tfheeler 1943; HaII 1974). Reid (1985) tisted several records of the species feeding on mistletoe nectar and fruit. However, the small amount of foraging for Mvoporum plelyç.arpum and $caevola gp!¡escens nectar $ras unexpected, because the plants bore small, highly scented, entomophílous flowers which did not contain visible amounts of nectar. Birds were probably more attracted to flowering X- platycarcum canopies by the numerous pollinating insects congregated there than by the possible nectar reward. Spiny-cheeked honeyeaters ingested small a¡nounts of the succulent young leaves of Lycium australe throughout the year but mostly in March and April, and were twice seen licking rain off foliage. Such behaviour is unreported for the species and proba-bly for honeyeaters Ín general. Other arid zone bírds, e.q. the black-throated spamow Àmphisoiza bilinegta (Smybh & Bartholomew 1966), Ieast seedsnipe Thinocorus n¡nicivorus (l'laclean 7976>, scarlet-chested parrot Nggphema splendide and inland dotterel Pe]'Lohvas australis (Schodde I98Ð, as well as desert rodents (Lee et aI. 1981) and macropods (Hain & Bakker 1981 ) often browse the leaves of grreen or semi-succulent plants, which contain sufficient water for the anÍmals to achieve water balance without drinking. Spiny-cheeks spent most time feeding on L australe leaves in March 1982 when most insects were eaten and relatively small amounts of tÍme were spent feeding on succulent fn¡its and nectar. Succulent fruits and nectar contain more water than insects, so the increased consumption of f, australe leaves may have compensated for the reduction in ç¡ater intake by birds eating insects. In a review of the quantitative evidence of dÍet in 28 honeyeater taxa, Pyke (1980) concluded that fruit played a negligible role in the diet of most species. only two species were recorded eating fruit. The lesser Lewin l,feliphaqa notata/graceful U- geecilis honeyeater ate fruit on 2L7. of. occasions, with 672 oE foraging observations on insects and only 18% on Page 130 nectar (Crome 797Ð. Ford & Paton (976) recorded 52. of observations of singing honeyeaters as taking fruit. The diet of the spiny-cheeked honeyeater at Míddleback, pooled over all seasons, consist-ed of nectar, fruits and insects in the ratio of 55%, 20% and 20% as determined by foraging observations and 40%, 20% and 30% on the basis of foraging tÍme (Table 5.3 ) . Nectar feeding constituted about 80% of foraging time in winter and spring during the long flowering season of AEvema quandanq. Fruits and insects contributed about equally to the remainder. $¡ith the exception of the small fruit component, the winter-spring diet resembled the highLy nectarivorous diet of the New Holland honeyeater Phylidonvris novaehollendiaC, Paton (1982a) found that New HoIlands depended entirely on nectar and alternative carbohydrates for energy, and only captured enough insects to meet their protein requirements. Non-breeding birds made about 100 foraging attempts daya for insects. Spiny-cheeked honeyeaters averaged 143 foraging actions day{ in the 1982 winter when most indivicluals did not attempt to breed. Assuming the two species had similar foraging success rates and captured insects of similar relative nutritional value, spiny-cheeks probably only captured enough insects in winter to satisfy their protein requirement. The fact that birds spent 86v. oE their foraging time feeding on nectar and succulent fruits rich in carbohydrate but not in protein suggested that they were more likely to be energy limited than protein limited. In summer, nectar vras a mínor component of the diet, the guantity of insects increased and Àmygme suandanq fruit were important. The time budgets suggested that spiny-cheeked honeyeaters increased their consumption of insects, or at least the number of foraging actions per day, by two and a half times. This is probably an overestimate due to the bias towards birds hawking insects, especially in March when the data were collected after heavy rain. Nevertheless, insect consumption çras higher in summer than Page 131 winter because the contribution of insect material to the voLume of solids declined by about half (Fig. 5.3) but the volume of solids in the faeces increased several times. Spiny-cheeked honeyeaters moulted between November and March, so the sunmer protein requirement would have been of the order of 502" higher than in winter (Paton 1982b). lJhether the increased consumption of insects exceeded their summer requirement is uncertain. The time burlget estimates of daily consumption of Amvema rruandang seeds were probably underestimates in November 1981 anrl Harch 1982 due to the bias towards foraging for insects. The January calculation of 315 seeds daya was not subject to the same bias and was therefore more accurate, The large number of seeds consumed presumably provided birds with most or aII of their daily energry requirements, Eurymelid honeydew may also have been important in early summer when fruit was not abunclant. 5.4.3.2 Population dynamics The long-term decline in spiny-cheeked honeyeater abundance encompassed a 3 yr period and was presumably related to the drought. The seasonal pattern in counts w¿rs linked to the changing abundance of the birds' major food resources. The high counts between autumn and spring coincided with the flowering season of À[yema quandanq. The lowest counts occurred in late spring when À- suandanq had finished floç¡ering but had not yet begrun the new fruiting season, and standing crops of fruit were virtually nil. Numbers increased over the summer to a February peak in 1981 and 1982 ç¡hen Lysiana elocarpi flowered. !- exocarpi largely failed to flower at the height of Lhe drought in early 1983, and honeyeater numbers remained atypically lor.¡ over the summer-autumn period until the first of a range of food plants began to fruit after the rains in late uarcn.8y' 5. 4. 3. 3 Territoriality Àlthough many honeyeater species display high levels of inter- and intraspecific aggression (Immelmann 1961; Bruce 1973; Ford 1979), the Page 132 existence of various systems of breeding and feeding territoriality has only recently become apparent (Recher & Àbbott 7970', Recher 1977: Smith & Roberts t978; Dow 1979a,b; Paton 1979: Ford s Paton 7982; Paton & Ford 1983). Keast (1968) described the spiny-cheeked honeyeater as a breeding resident over much of Íts southern Australian distribution, noting that part of the population in some districts undertook nomadic movements. Pairs held year-round territories at Middleback, which they defended for feeding and breeding purposes when food was locally sufficient. In good years ç¡hen food was continuously available, pairs probably resided in territories year-round. In summer in seasons when food was scarce, birds spent much of the time off their teritories in search of food, but revÍsited them periodically and foraged. S¡riny-cheeked honeyeaters were dependent on the nectar and fruit of Amvemq zuendanq for most of their energry requirements. Paton (979; Paton & Ford 1983) showed that New Holland honeyeaters and red and little wattlebirds had comparable carbohydrate dependent ecologies in dry sclerophyLl forest and wet heath habitats Ín Victoria, and that they adopted short-term feedíng and breeding territories because of seasonal changes in the dispersion of nectar and alternative carbohydrates. The species depended on a variety of food plants and had to shift territories between patches of appropriate plants as a succession of carbohydrate resources peaked one after the other. The habitat of the spiny-cheeked honeyeater in the study area differed in that one plant species provided most of the carbohydrate reguirements of the species throughout the year. Accordingly, birds tended to occupy one area continuously and remained faithful to their territory from one year to the next. The size of the territories was such that some of the minor food plants used by spiny-cheeked honeyeaters occurred in each pair's territory. The site fidelity of spiny-cheeked honeyeaters at Hiddleback has analogues arnong honeyeater species in temperate and subtropical eastern Page 133 Àustralia. tJhite-eared honeyeaters llqhenostomug leugotis possibJ.y reside year-round in territories of about t ha in dry scJ.erophyll forest north of Sydney, Ner¡ South tlales (Recher & Àbbott t97Ð. Noisy Ma¡q¡lna melanocephala and bell M- mefanophfyg miners form colonies in euclalypt woodland and forest in eastern Australia, which persist for many years (Dow t977, 1979a,b; Smith & Robertson 1978; Lloyn C! aI. 1983), AII three species probably depend on lerp and other carbohydrates for theÍr energy requirements (Paton 1980; Llykes 1982; Lloyn C! aI. 1983). Territoriality in arid zone honeyeaters has not been previously described, However, a number of species other than the spiny-cheeked are common residents in the arid zone (Keast 1968; Brooker e! eI- 19791 Shurcliff 1980), including the singing honeyeater and yellow-throated miner [- flaviqulq at Middleback. Preliminary data indicate that individual singing honeyeaters are sedentary and exhibit site-specific aqgression. 5 .4.3. 4 Breeding Schodde q982) reviewed evidence concerr¡ing the breeding of arid zone birds in Australia and drew three conclusions:- 7. There is a consistent major peak of breeding Ín spring (August-0ctober) in nearly all species and a minor one in autumn (Àpril-May). Autumn breeding only becomes important when drought that depressed spring breeding is broken by summmer rains. 2. There is a significant pause in breeding during winter due to the inhibitory effect of cool weather on spennatogenesis and to a lack of food. 3. The extent of spring breeding varies according to the amount of rain that has fallen in the preceding summer, autumn and winter.. If little or no rain has fallen, breeding is depressed. The pattern of breeding in spiny-cheeked honeyeaters at l'liddleback conformed closely to 1. and 3. Spring breeding occumed in each year, and was most successful in 1980 and 1983 following moderate to heavy rainfalI. Page 134 Little breeding was attempted in the 1982 spring due to the drought. Following the good season ín t979, there was no evidence of autumn breeding in 1980. Following the 1982 drought, rain in March and April 1983 ç¡as followed by almost immediate egg-laying. The only discrepancy was the lack of evidence for a cessation in breeding in winter 1983, contrary lo 2, The relationshjp between breeding, seasonal conditions and food abundance was not straight-forward. The drought-breaking rains in March and erarly ApriÌ 1983 resulted in abundant Amyema guandanq fruit by the end of March (Fig. 4.2) and the appearance of Rhaqodia spinesgglg, Exocarpos ephyflug and lnchylaena tomeDtose fruits by early or mid April (Fig. 4.22), Spiny-cheeked honeyeaters responded with immediate breeding activity. An excellent year in 1979 and the large rain in April 1980 produced similarly jntense breeding activity in the spring of 1980. However, no breeding was observed in June or early JuIy 1980 when there stere moderate amounts of E8ocarpos aphyllus, Enchyleena tomentosa and probably Chenopqdium qaudichaudianum fruit available, as well as abundant Amvgma SJqldanq flowers. The difference in timing and duration of breeding between 1980 and 1983 may have been related to conditions in the preceding years. Large rains occurred throughouL 1,979 and honeyeaters presumably bred successfully, resulting in the high density found in spring 1980 (Fig. 5.4). By contrast, 1982 was a drought year, few birds attempted to breed and the population density had declined significantly by the end of the drought. There was presumably a selective advantage for individuals to produce young as soon as conditions permitted after the drought, while the population density remained low. However in 1980, when previous good seasons had all.owed the population to build up, there was probably no advantage, and perhaps a disadvantage, in breeding except under putal-ively optimal conditions in spring. Page 135 5.4.4 Histletoebird 5.4.4.1 Diet l'he diet of the mistletoebird at Middleback ç¡as dominated by mistletoe fruit. The large number of seeds eaten (274 1 25 seeds dayr) and the large amount of foraging tÍme spent searching mistletoe canopies jndicated that the species was dependent on mistletoe seeds for its energy reguirements. The 40% increase in seed consumption in winter may have been related to the increasecì thermoregulatory costs incurred during cool weather, and the few insects eaten (67 1 29 f.oragíng attempts daya) probably only satisfied the species protein requirement. March 1982 v¡as the only month in which foraging time for insects was similar to that for fruit feeding (Fig. 5.7Ð. Amveme ggandanq fruit were abundant in March (Fig. 4.Ð. The foraging efficiencies of both mistletoebirds and spiny-cheeked honeyeater.s, in terms of the number of seeds ingested per minute and the ratio of seeds ingested to the total number of pecks at fruit (Tables 5.7 u 5.11), $rere higher than in other months. Birds therefore spent less time harvesting their daily fruit requirement than in other months. Canopy dwelling insects may also have increased in response to the heavy rain in late March, in parallel with the increased abundance of flying insects. Mistletoebirds maintained a higher rate of wing-flicking and made more foraging actions per minute for insects than in other months. Thus the relative increase in foraging time for insects probably re.rulted from a temporary abundance of insects coupled with an abundant and readily harvestabJ.e supply of ripe fruit. The rariby of insect remains in mistletoebird faeces is enigmatic. Liddy (7982) found no chitinous remains of arthropods amongst the mistletoe seeds defaecated by 92 birds. I found macroscopic remains in only two seed-strings (0.5%) and microscopic remains in another three. The ghortfall jn defaecated material corroborates Desselberger's (1931) observation that chitinous remains do not occur in the intestine, prompting him to suggest Page 136 that indigestible matter was reçfurgitated. However, in many hours of observation, I never saw mistletoebÍrds regurgitate pellets. The possibility remains that pellets were ejected at night. Àn alternative hypothesis is that arthropods are usually completely digested in the stomach. Material in the diverticulum gizzard presumably does not impede the passage of berries through the grut, so there is no necessity for relatively indigestible material to move quickly out of the stomach as in birds with a more typical digestive anatomy. Exoskeleton could be pulverized and eventually absorbed along with other arthropod parts if food remained in the stomach indefinitely. 5.4.4.2 Influence of diet on life history The year-round production of fruit in the Arnyemg cnrendenq population ena-bled mistletoebirds to occur at Ì,fiddleback throughout the study, and permitted some individuals to reside locally for many months. Blakers et qL (1984) examined the regional movements of mistletoebirds across the continent and concluded that, because broad scale popuJ.ation shifts were absent, Iocal nomadic movements must keep the species in contact with fruiting populations of mistletoe. Most mistletoes do not fruit throughout the year (Reid 1985), so the fruiting seasons of sympatric species are presumably staggered in most areas and provide a year-round supply of berries. This is the case in both the temperate and arid regions of South Australia (Reid 1985). Keast (1958) described the mistletoebird's long breeding season on the plains at the base of the BIue Mountains, west of Sydney, where the fruiting of three species of mistletoe was staggered, providing food in both spring and summer-autumn. A similar sÍtuatíon pertained at Middleback except onl.y the one mistletoe species was invol.ved: spring egg-laying between JuLy and September occurred as the last of the old fruit crop rípened, and mid sufluner breeding coincided with the cornmencement of the new fruiting season Page 137 between November ard January. Breeding occurred at a time of low fruit aburdance in spring 1981, as well as at high, indicatíng that fruit abundance as measured by standing crop had at best a partial role in initiating nesting. The fact that fn¡it was availabLe throughout the year but mistletoebirds only bred in spring and mid summer also indicates other factors must be involved. Hore detailed studies of the factors controlling breeding would be desirable. Despite the dependence of mistletoebirds on Amvema quandang fruit at Middleback, temporal trends in mistletoebird abundance bore no relationship to the standing crop of fn¡it. À linear relationship between fruit production and mistletoebird abundance would be expected if fruit was Iimiting, and mistletoebirds were the only consumers of the fruit crop. However, spiny-cheeked honeyeaters ate much of the fruit in summer (section -/.t.3.2) and there was little evidence to suggest that fruit was limÍting mistletoebird abundance at any stage. Standing crops are a function of production and removal. A simple rel.ationship between fruit production and standing crop did not occur because removal rates of A- quandaDg fruit varied throughout the year (section 7.1,3.2). Accordingly, the absence of a relationship between standing crop and mistletoebird abundance was not surprlsrng. 1.t Page 138 Table 5.1 Definition of the five modes of avian foraging behaviour with respect to the position of the bird ar¡d food item. Bird Àirborn Perched Sally Snap Food Item Snatch Glean Srntch hobe Table 5.2 The number of faecal samples from mistnetted birds in the trapping area, which contained mistletoe seeds in 1980-82. The figr-rres in parentheses are the number of faecal samples obtained from each (LE). bird species. Amyema qgqndang seeds (AQ); lygiana exocarpi Bird species Dec 80 Nov 81 Jan 82 Mar 82 Ì'fay 82 JuI 82 Sep 82 Nov 82 Total (1) pigeon 0 (1) 0 Crested (1) (1) Black-eared Cuckoo 0 0 0 (1) 0 (1) 0 (1) 0 (3) Red-capped Robin (1) Rufous Whistler 0 (1) 0 0 (1) 0 (1) 0 (2) 0 (4) Grey Shrike-thrush (1) (1) Crested BelLbird 0 0 t{ilIie tiagtail 0 (2) 0 (2) (3) (13) (4) 0 (2) 0 (9) 0 (16) 0 (10) 0 (57) White-browed Babbler 0 0 0 (6) Variegated Fairywren 0 (2) 0 (4) 0 (3) 0 (2) 0 (2) 0 (7) 0 (2) 0 (1) 0 (17) Inland Thornbill 0 (8) 0 (4) 0 (1) 0 (2) 0 (1) 0 Chestnut-rumped Thornbill (16) 0 (7) 0 (3) 0 (6) 0 Yel low-rumped Thornbi I I (4) 0 0 (1) 0 (1) 0 Southern tJhiteface (2) Red Wattlebird t" 0 (1) 0 (1) 0 (4) (8) (11) (9) 28 (56) Spiny-cheeked H'eater AQ 5 (6) 7 (7) I (9) 3 1 1 3 0Q) (1) 0 (2) 0 (2) 0 (2) 0 (3) 0 (7) 0 (17) Singing Honeyeater 0 (1) low-plumed Honeyeater 0 (1) 0 Yel (4) (2) (4) (13) AQ 3 (3) 3 2 2 10 Mistletoebird (2) (4) (13) LE 0 (3) 2 (4) 0 0 2 0 (3) 0 (3) Grey Butcherbird I'Þ ao (¿) \o Page 140 Table 5.3 Proportions of the main components in the diet of the spiny-cheeked frãnãVãater. Data are the avèrage of percentages for each month. Technique Period Nectar Insects Fruit Honey- Other' dew Foraging observations 1980-83 54.1 18.9 21.9 1.5 3.5 (n = 4177 actions) Foraging observations Nov. 81- 48 .6 22.9 20 .6 4.t 3 . 9 (n = 1668 actions) Oct. 82 Foraging time Nov.81- 42.9 33.1b t9 .2 3 .7 7 .2 (n = 23909 s) Oct. 82 .tycium auslrale leaves and rain ticked off foliage. t Iñõfuae= tJrnelerchted and Iooking between consecutive sallÍes. Table 5.4 Diet of the spiny-cheeked honeyeater at Hiddleback, 1980-83. Data are percentages of the monthly lotal of foraging actions. sampfe sizes are shown in Figure 5.1. ; Exap, Exocarpos aphvllus; HeoI, Heteroderdn¡n ya.r, Lvcium australe; Lyex' Lvsiana gxocaEpÅ; Rhsp, JFHAHJJÀSOND AÍqu 6.7 22.0 86.3 77 .8 79.7 86.0 85.5 43.5 31 .3 Floral nectar Lyex 0.7 34.{ 6,1 'o-' Hvpl 5.3 2.7 7.7 ÀÍqu 55.4 43.8 8.3 29 .7 t_, 0.1 7.7 0.5 22 5 36 :s Chga 0.7 7.6 Ento o:, 11 .0 1.5 3.9 4.4 rlt Fnrits Exap 1.0 6.9 t_, 1.7 t:t HeoI o:t Lyau '-o 2.8 Lyex 7.4 t.L Rhsp 4.3 9.4 0.9 Trees & shrubs 13.0 1.0 8.3 15.0 2.4 7.7 t:, 2.9 3.9 4.4 1.5 20.9 Bust¡ sPP 0.7 1.7 0.4 0.4 o._, 0.3 3.4 Insects Sallies' 73.7 18.8 48.9 o:, ,:o 8.9 2.9 3.9 o:t t:o u:, C'rûUrd 5.0 7.7 0.3 o.2 Ìliscellaneous 0.7 0.8 0.3 0.9 0.3 HoneldeeÞ 2.9 15 .0 Other Lyau leaves 3.6 ,:t 14.4 7.9 4-.g n:t 2.7 H€ from foliage 0.9 0.6 'lt 0 ao .sallies in free airspa.ce beyord plant canopÍes. àsecreted þ eurymelia ¡r-,gs ón new foliage of Heterodendrum oleaefoliun. À Paqe 142 Table 5.5 Foraging behaviour and sites where spiny-cheeked honeyeaters foraged for insects at Middleback. Data are percentages of. 574 foraging actions. Foraging behaviour Height Glean Snatch Snap Sal ly (Foliage / Branch) ( In canopy/mid air) Ground 4.2 Bush 3.5 / 0 0.2 / o o / 4.2 Tree 8.4 / 77,0 5.7 / 0.9 7 7 5.9 / 33.4 Àbove 8.0 Not recorded 72.9 Table 5.6 Seasonal behaviour of the spiny-cheeked honeyeater foraging for insects. Data are percentages of total foraging actions in each month. Month Behaviour J F Ì'f A M J J À S 0 N DÀve Sat1y 4t 95 88 44 76 85 44 57 31 t7 62 2t 55 Snatchlt-746299742811159 Snap25tt63--32-3 Glean/probe 46 10 36 15 13 47 35 54 52 24 65 33 (Sample (46) (19)(106) (25) (33)(9?,) (45) (23) (14) (29) (45) (34) size ) Page 143 Table 5.7 I'ime budgets of spiny-cheeked honeyeaters at Middleback. Nov 81 Jan 82 Har 82 May 82 JuI 82 Sep 82 Total time (s) t9825 8510 9724 9277 12339 74448 % Time foraging 41.7 39.9 28.7 44.6 37.7 54. 3 Insects % Foraging time 37 .4 43.4 75.5 6.7 26.0 10.1 No. of foraging actions/min 1 .89 2.12 2.83 5.28 3.36 2.77 Sample size' (s) 1869 876 2054 250 1 054 47t No. of foraging actions/day 245 308 454 90 197 113 Àmyema quandang FrUit % Foraging time [t.t 53.1 10.3 t.6 No, of foraging actions/min 4.37 5.77 4.05 4.29 Sample size' (s) 1015 847 74 t26 No. of seeds consumed/day 101 315 36 10 Ratio of seeds consumed to no. .16 .34 .40 .33 forag. actions Àmyema guandang Nectar 7" Foraging time .t .7 93.9 72.8 86.3 No. of probes/min 50.0 24.9 32.4 30 .2 24.5 Sample size' (s) 6 20 1 568 1 036 2644 No. of probes/day 13 36 8555 4969 8496 Honevdew Lysiana exocarpi flruit % Foraging time 19.0 3.0 % Foraging time 1, ,2 .5 No. of licks/min 16.0 4.0 No. of foraging Sìample size' (s) 814 60 attempts/min 2.78 9.73 No. of licks/day 1 049 40 Sample size' (s) 55 37 No. of secds cc,nsumed/day 5 0 Lycium australe Leaves % Foraging time .3 .5 5.9 No. of leaves consumed/min 24.5 6.7 20.1 Sample size' (s) 22 18 164 No. of leaves consumed/day 20 tt 253 "No of seconds of observations used to calculate the foraging rate. Page 144 Table 5.8 Composition of the solid fraction of faecal sanples from spiny-cheeked honeyeaters. Data from mistnetted birds ard field collections are pooled. Samples not fourd in the field appeared to be mostly fluid with little or no solid material. ÀbbrevÍations of plant rìarnes are listed in the legerd of Table 5.4. JFHÀMJJÀSOND No. of samples 27 72 74 10 t4 t6 1 76328 (No. not found) (3) (8) (2) (1) (5) (2) : Ànqu .95 1 .0 ,79 .80 .74 .43 .06 - .50 .67 .86 .89 9.3 71.7 A.2 3.5 0.1 0.6 0.2 - 2.3 4.0 7 .3 9,7 Lyex - .10 .27 .71 .79 - .06 - .20 .20 .90 .40 - .10 Ento - .s0 .74 .38 - lo .67 .7t .22 Proportion - 2.6 0.4 .80 - .80 9.0 .10 1.9 containing fruit Heol 05 .29 remains 00 .10 and Exap .24 .08 .47 .14 .74 .38 1 .0 .38 .33 .11 1.0 .30 .10 .10 .30 1.6 9.0 4.3 .30 .50 I'lean no. of seeds/ Rhsp .74 - .14 .60 .21 - .77 sample 2.9 - 1.3 6.7 .30 - .30 Chga .05 .13 - .06 - .11 .10 .40 - .10 - .70 Lyau .10 07 .60 60 Àcos .05 .20 Lyau .05 .57 .10 .74 .79 .06 07 Ieaves Proportion cont- Insect .77 .77 . 86 . 60 .64 .29 .88 1 .0 .81 .67 .43 .89 aining: re¡nains Urates .43 .58 .43 .50 .50 .50 50 .67 .43 1.0 Ta-ble 5 .9 Contents of spiny-cheeked honeyeater faecal samples obtained from mistnetted birds at four-Ioäalitíes on Uíddleback Station, 1980-81. See Table 5.4 for abbreviations of plant names. Scar, Schinus argira' l'roportion containing fruit remains Proportion Locality No. of (Hean no. of seeds Per samPle) containing & Date Samples Lyau Insect Àmqu Ento ExaP Heol Scar Chga leaves Urates remains Extension 3 .33 .67 .33 .33 1 .0 tror-rgh, (.7) (3.0) (1.7) 20-21/8/89 tledge Corner 72 .58 .77 .33 .75 paddock (4.7) (.3) 73/9/80 Shearers' 28 .71 .07 .77 .61 gtrarters, (.8) (.1) 72-73/70/80 l,fid-western 4 .25 1.0 .25 1.0 1.0 Overlard pa.d. (.5) (3.8) 72/2/87 -o I ao À (.ñ a Page 146 Table 5.10 Regression analyses of spiny-cheeked honeyeater and mistletoebird census counts on (À) time and a pair of annually cyclic variables, and (B) f,gyegq qgandq¡çI (ÀQ) and Lreigna e¡aqeEp¡ (LE) flower and fruit abundance. Data for ie) spanrred Àugust 1980 - JuIy 1983, and for (B) March 1981 - July 1983. TIME measured in days. Dependent Independent F-ratio t' Significance of variable variables (d-L) mrtial regression coefficients (A). Spiny-cheek T IME 13. 625r(*x . 55 x1*** countsb' X1 (3,34) xi*** 11'2 x2*** Mistletoebird TIME 5.472x .13 countsb d (1,36) Mistletoebird À1 4,197* .t9 xr NS ( countsb " Xz 2,35 ) xz* (B) Spiny-cheek AQ flowers (xs) 5.817x* .50 w-** counts AQ fruits (x1) ( 4 ,23> xr NS LE flowers (x:) xs NS LE fruits (xc) xs NS Spiny-cheek AQ flowers (x¡) 24.69txxx .49 countsr (7 ,26) "The annually cyclic functions used ín analysis were: Variable Period (d) Function xr 365 Xr = coS( 2t x 11Y6/365 ) x2 365 xz= sin(21 r( TIME/365) No q pfigEi assumption was made about the initial phase of the seasonal variatloñ, so both varj.ables were retained in analyses irrespective of the significance of the partial regression coefficients. bThe bird count data were trarrsformed to their natural J.ogarithms. rlhe regression equation was: ln y = 3.426 - .0008TIHE + .38É,xr - .331x2 dlhe regression equation was: lny-7.514-.0006TiM8 "Ihe regression equatÍon was: ln y = 1.18 + .!27n+ .332x2 rlhe regression equation for the untransformed data was: Y=16.499+.067xt Paqe 747 Table 5.11 Time budgets of mistletoebirds at Ì'fiddleback Sep/ Nov 81 Jan 82 Mar 82 May 82 JuI 82 Oct 82 Total time (s) 4890 4580 681 9 11018 7153 8968 % Time foraging 24.6 29.3 22.3 29.4 36.2 27.7 J.ngec!g % Foraging time 6.2 29.4 55.6 7.7 20.3 18 .5 No. of foraging actions/min .80 .37 2.23 1.67 1 .80 1 .88 SampLe size' (s) 75 326 647 257 467 351 No. of foraging actions/day 10 27 205 24 81 56 No. of wing- f1 icks/min 0 n.r. b 18 I 13 7 Amyema quandang Frui! % Foraging time 93.8 70.6 44.4 84.8 61 .5 79.9 No. of foraging actions/min 2.37 4.57 5.55 6.32 7.71 4.46 Sample size' (s) 447 446 573 2032 747L 1210 No. of seeds consumed/min .68 r .35 2.62 r.77 7.67 7.29 No. of seeds consumed/day 130 235 192 278 227 166 Ratio of seeds consumed to no. .29 .29 .47 .28 .22 .29 forag. actions Lysiana exocarPi Fruit % Foraging time 7.5 78.2 No. of foraging actions/min 1.48 1.27 Sample size' (s) 243 471 No. of seeds consumed/min .74 1.15 No. of seeds consumed/day 10 46 Amyema quandang Neclel % Foraging time 1.5 No. of probes/min 6 Íìample size " (s) 30 used calculate the " The number of seconds of foraging observations to foraging rate. bn.r., not recorded Page 148 Table 5.12 Foraging behaviour and sites of mistletoebird foraging actions for insects (n = 81). Table entries are percentages. Site Foraging Behaviour Snatch Glean Saliy FoI iage 4.9 19.8 Branches 8.6 42.9 Space wÍthin 21.0 canopies AÍr space 3.7 beyond canopies Tab1e 5.13 The numbers of mistletoe seeds in mist.Ietoebird stooLs collected or examined in tne fie]d, 1980-1983. Amqu, Àmyema zue¡den ; Lyex, Lvsiena exqqerni; Hist., either species. No. of No. containing No. of seeds Month stools seeds of I t s.e. (range) Mist. Amqu LYex Amqu LYex Jan t7 77 t7 2.5 ! 0.23 ( t-4) Feb 7 7 t 2.0 Mar t6 t6 t6 2.6 ! 0.50 ( 1-9 ) ( Àpr 10 10 10 3.0 t 0.44 1-5 ) ,) ( ( J 2.7 0.33 0-5 ) 0.2 0 .08 0-1 ) May 20 20 18 ! ! (0-2) 77 7 1.9 ( 0-5 ) 0.1 1 0 .!4 Jun 74 t2 10.40 (0-2) JuI 22 2t 77 5 2.6 ! 0.46 ( 0-7 ) 0.4 t 0 .77 ( Aug 7 5 5 1.6 10.s3 0-3 ) ( sep 47 39 39 2.8 ! 0.16 0-s ) 0ct t6 15 15 2.8 ! 0.28 ( 0-5 ) ( Nov I 8 I 3.9 1 0.s2 2-6) ( Dec 10 t0 10 2.2 ! 0.29 1-4) Totals 182 774 767 9 2.6 t 0.tl ( 0-9 ) Page 149 Tab]e 5.14 proportions of the main components in the diet of the mÍstletoebird. Data are'the average of percentages for each monthly (Nov. 1981 - Oct. 7982) or two monthly (1980-1983) Period Technique Period Fruit Insects Nectar Foraging observations 1980-83 85.0 72.5 2.6 (n = 738 actions) ForagÍng observations Nov 81 - 88.5 7t .t 0.4 (n = 581 actions) Oct 82 Foraging time Nov 81 - 76.8 ?3.0 0.3 (n = 1.1844 s) Oct 82 Table 5.15 the comparison of the quantities of Àmvema sJeEdenq_seeds and insect remains Ín faecal samples from ãliñr-"n"eked honeiðã["r. sampteJiEõ õtte"t.a in the field and from mistnetted birds between November 1981 and Ì'farch 7982. (%) No. of Àmvema quandanq seeds Insect remains Time of collection Ìlonth Stools Freguency No. of seeds 1 Volune Freguency % Volume Morning Afternoon (7.) XtS.E. 1ç+S.E. ("¿) i t s.n. Early Late EarIY Late 35 November 15 87 8.2 t 1.8 70 ! 10 53 26 +9 15 10 40 1981 January t6 94 70.2 ! 7.7 68 t 10 77 24!70 38 25 13 25 7982 l{arch t2 92 4.9 11.0 58 18 100 29 +4 15 23 31 31 7982 -u qø o oCN J T M A M J J A S o N D PAgE151 EE MISCELLANEOUS INSECTS E¡= FRUITS E =rIIIr NECTAR J F A M J J A S ON D fl 39) (l 80) (358) (376) e2Ð (333) (96) ( 27i--(r366) (306) (s46) flI5) No. of foraging attempts Fig. 5.1. Main components of the diet of the spiny-cheeked honeyeater, 1980-83. Height of the bars is proportional to the number of foraging actions. Unshaded porbions of fruit and nectar bars represent feeding actions at Àmvema quandanq. Sample sizes in parentheses. Page 152 KEY lnsects & Miscellaneous Fruits & Nectar Eurymelid honeydew ffi Lysiana exocarpi Rain licked from foliage Exocarpos aphyllus Lycium australe leaves m in tree canopies Amyema quandang in bushes/ on ground Myoporum platycarpum lnsects sallies Heterodendrum oleaef olium time perched between sallies Fig. 5.2. Diet of the spiny-cheeked honeyeater as determined by percent foraging time from time-budgets (TB, Ieft column of each pair) and from foraging observations (F0, right column of each pair). Height of the bars is proportional to seconds of foraging and number of foraging actions, respectively. Timed foraging bouts in which more than one item was procured are indicated partway between the respective categories. Sample sizes in parentheses. Foraging time(s) (3 (8262) (3398) (2795) (4 I 08) (4578) (7839) r68) SEP/ JUL82 NOV82 NOVS r JAN82 MAR82 MAY82 ocT82 MISCELLANEOUS ffi ffi INSECTS N % TB FO TB FO TB FO TB FO TB FO TB FO TB FO FRUITS NECTAR ffit ß dt NOVS I JAN82 MAR82 MAY82 JUL82 SEP/ NOV82 ocT82 ( (353) (33 I il 59) (l 99) (99) r 55) ) (53 l) No. of foraging attempts (6) (7) (9) (4) (8) ( lo) (9) KEY A Amvema ouandanq seeds N -r- Seeds & fruit remains N of other plants N o Other Plant material N lnsect remains A A N A I u,.t,, A Minerals A DEC NOV JAN MAR MAY JUL SEP 80 8l 82 82 82 82 82 Fig. 5.3. The mean compositiol, by volume, of the solid fraction of Samples were honeyeatei faecal samples between 1980-82. -ú =pí"t-¿n;eked paddock study area. sample obtained rrom misi.r"[t"a birds in tire Overland aÞ sizes ín parentheses. o (¡tl qJ Page 154 10 Mistletoebird U' J J o o o z_ 50 TL Spiny-cheeked Honeyeaters o 40 zcj 30 f-a \ 20 \ 10 o D o DfA AO D AJ 1 980 198 1 1 982 1 983 TIME Fig. 5.4. Census counts of spiny-cheeked honeyeaters and mistletoebirds along the 3.3 km traverse in Overland and Railway paddocks, AII indivÍduals (continuous line); indíviduals in woodland, excluding those flying over (broken line). 40 a a a a 30 a a a U)o fr a a d) 20 ol! a a d o a z a 10 a o 50 100 150 200 250 NO. OF FLOWERS Fig. 5.5. Relationship between numbers of spiny-cheeked honeyeaters and abundance of Àmyema guaDdang flowers (mean number of flowers per plant) along the traverse, 1980-83. The curve was fitted by eye. Page 155 JFMAMJ JASOND I o- o o ¡ o o 1 980 o o o o 2n o-d - 2n-t -t 1981 o-d a x o-d x I-€ o--l 1 982 a a TX otr Inxx a o¡atr.otr .Eb-r O--HI - 1 983 a- --tr JTM AMJ JAS OND KEY . Collecting Nesting Material o Nest Under Construction o Nest With Eggs r Nest With Young o Dependent Young Out Of The Nest x hdependent Juveniles n Nest With Unknown Contents ,- n -, Nest Constructed in This Period d Nest Abandoned (Predated or Deserted) Fig. 5.6. Breeding seasons of the spiny-cheeked honeyeater at l{iddleback bei,ween 1980-83. PerÍods of fieldwork are irdicated by the black bars on the datelines. Symbols linked by a line refer to the same clutch or brood. Synbols linked by a broken line refer to different clutches or broods of the one colour-barded fernale. Data for colour-banded birds are sho$tn below the dashed line in 1982 ard 1983. Page 156 Fig. 5.7. ÀII records of two mated spiny-cheeked honeyeaters, Bu/I{ (female, upper row) ard O/td (mate, lower row), in the trapping area between November 1981 - January 1984. KEY o Perched, singing Feeding on food plants, ^ principally Amyema quandang o Agonísticinteraction v Perched . ..- Display f light t t I I I I I 82 t6 ST -to I I I I I I W o fl ü v Foraging alone Usually with 0/W r Banded lO/ I I /81 o Colour-banded l5/ I /8? 1 ¡ Retrapped l8/5/82 2 3 o r Banded I 5/ I /82 o Retrapped & colour-banded t 5- t6/5/82 2 3 t I I I 2 I 6- PT I I 7- a2 I I I I I I I v g v I ^ v Â^ VV Foraging wlth O/W Early a.m. : alone Usually with O/W o Displaced bY O/W o Evicted by unbanded male 4 lrom flowers 5 6 7 2 2 v ^ o With BulW Sometimes with BulW oEvicted from honeydew 4 5 laden tree bY O/Bu 6 I I I I t6 L-5 83 I I I I o& Mainly with O/W Late p.m. : with O/W; r o s inging intermittentlY I Nest,2 e s, l8/4/83 I I I I I I I I I I I I v A A v Alone searching mistletoe Late p.m. : foraging Vocal &. aggressive ¡ ca nop ies 7 in mistletoe canoPies 8 often with BulW I Page 157 I ü v With juvenile af ter fledging r rìoSt, young, Sometimes with 0/W I Mid p.m. : with O/W 10 fledged 3/8/83 11. 12. -28 T Mostly with Bu/W; af ter 3/8/83 with fledgling Mostly with BulW o Evicted a Spiny-cheek 10. & Singing Honeyeater 11. 4 Early a.m. :foraging alone o Retrapped 3l/l/84 13. s3 ¡t Mid a.m.:alone, searching mistletoes . Retrapped l6/ I /84 13. Paqe 158 to v ô 9 o 9A G/O band. m. Tuft IX X I v ^ unb. f. Bu/Ba Bu/O unb. m vlll V I I vv9 I 99 I W/Ba Bu/W vv  Â & I Bu/G o/w I VI Fig. 5.8. The movements and activities of five pairs of spiny-cheeked hoñeyeater containing at least one colour-banded bird and of a lone irdividual (Tuft) in a sixth territory, over 3 d in June 1982. Symbols as in Fi9.5.7. Page 1,59 o$ o vv o A A o A V. ^a v o a o vvv il A^^o o Y ^^ VV A %'â^x.õ. o A AL ¡ ^ V v'fl v ^^ I o A I X I a O¡ I o I o I II o rl I o or v T lil t I I È tl ¡l o Fig. 5.9. Distribution of spiny-cheeked honeyeater territories in the trãpping area in June 1982. Closed symbols are where members of a pair fed at lóo¿:plants or sang, open symbols where they perched, and dotted symbols in territory XI where three adults were seen together. The small squares of the grid are t ha, Page 160 o I a0 o O. íî. I ó0r-9 I 6'o a ' ;&. I I al .t !.'n o B I a '0 I û'I I oof a o Þo o ,,rê Cî o .a o t o /o oo ô b ô o a ,o.a o- I ê ê ù ioo Þ 0t: .4 ( o c êc c.e a ô og' 0 of .e-. O o o E o a 4 o o f 0 o ( a tc à' o t o :":I þoo a Þ o ,l o .'q o ¿O t .aQtO a- o ér tt,oo q0 a ,.t o , ô oo ,ô a a t, ô' o GI s oâ C' oo I e:t go. t ro e.o L, t-.6 jog o rÞ o 9 I O.¡ r0, I oS o' /c o J o o s o 1¿ .,o.P io oo I b '96 .l o fô o, a"p' o lo'o'O P oorô'J öa ot ,êd o t¿o ' .r" tt d u'. oo , ô ;.:'f* i,,.-,, a0 c a o s o' 0"a a s ô O.. o.. to o o 'ô.' ',¡ -' F O. l. c O '.' l. cP :,' 1. Fig. 5.10. Distribution of tree and shrub canopies in the trapping årea. The small sguares of the grid are t ha in area. Page 161 DEC_ MAR APR_ JUN_ AUG_ ocT- JAN MAY JUL SEP NOV NSECTS FRUIT NECTAR DEC- MAR APR- JUN_ AUG- ocr- JAN MAY JUL SEP NOV (61) (72) (1 ee) (1 e5) (11e) (s2) KEY T Amycme-quandang- ffi Lysiæac¡ocarpj I E-ra.cat P is-e P-þ Y I I u s Ø lnsects captured in tree / tall shrub canopies N Sallies,beyond canopies Fig. 5.11. Diet of the mistletoebird as determined from foraging observations at Middleback betç¡een 1980-83. Height of the bars is proportional to the number of foraging actions. The total number of foraging actions recorded Ín each t or 2 mo period is shown in parentheses. Page 162 KEY Amyema quandang ffi LVsiana exocarpj I E x oc arp o s_Ap¡y llu s ffi We stern myall yp p-orumj.lat y têrp un Ø M N Heterocle n clru m oleaefolium m Other tree & shrub canopies Fig. 5,72. Diet of the mistletoebird at iliddleback as indicated by percent foraging time from time-budgets (TB, Ieft-hand columns), and foraging observations (F0, right-hand columns). Height of the bars is proportional to secor¡ds of foraging and number of foraging actions, respectively. The insect component is subdivided into the species of tree and shn-rb in which foraging occurred. Foraging bouts in Àmvema quandanq in which insects and fruit or nectar ar¡d fruit stere sought together are indicated by bars midway betv¡een the respective categories. Sample sizes are indicated in parentheses. Total numberof seconds f oraging ( 141 5) (1 ( 1 201) u342, ( 1 52 1) ß241, |..¿57 0' 1s0) ocr NOV 82 NOV 81 JAN 82 MAR 82 MAY 82 JUL 82 SEP 82 DEC INSECTS NKN TB FO TB FO TB FO TB FO TB FO TB FO TB FO FRUIT ìi: !4.1 NECTAR ttrtlll 'ocr I NOV 81 JAN 82 MAR 82 MAY 82 JUL 82 SEP 82 NOV 82 (26) (37) (70) (217, ( 1 2e) (62) DEC (66) Totalnumber of f oraging attemPts Page 163 JASO NDJFMAMJ 1 980-8 1 o a o o o on x )(x 1981-82 tr x o o aaa x 1 982-83 a oo x 1 983-84 o a o ¡ J ASONDJF MAMJ Fig. 5.13. Breeding evidence for mistletoebirds at Hiddleback, 1980-84. Key tó-åvm¡ofs as in Fii. 5.6. The black bers on the datelines indicate periods spent in the field. CHÀPTEII 6 BREEDING SYSTEM ÀND POLLINÀTION ECOLOGY OF ÀHYEUÀ QUÀNDÀNG a 6.T BREEDING SYSTEM AND POLLINÀTORS 6.1.7 Introduction Breeding systems are not distributed randomly among the plants of different habitats (Lloyd 1980). One association which has often been noted is that between self-fertilisation and fluctuating, unpredictable and harsh environments. The advantage of self-fertilisation is an increased success in fertilisation, and in an unpredictabl.e environment, self-fertilisation is a fail-safe system ensuring some seed wiII be produced despite pollinator failure (Keighery 1982). The arid zone unpredictability hypothesis asserts that the desert areas of Àustralia are an unpredictable habitat for plants and animals because of the erratic nature of precipitation patterns (section 7,7). Therefore, one might predict that the breeding systems of arid zone plants should favour self-fertilisation. The breeding systems of Àustralian species of Àmyema are variable (Table t,t), and the genus provides a useful test of this prediction. Bernhardt eL eI- (1980) showed that a temperate population of f,- q¡andanq in Victoria was self-fertile and facultatively out-breeding. Thus the unpredictability hypothesis would predict that an arid zone population of the same species should exhibit a tendency towards obligate inbreeding. This chapter describes the breeding system and pollination ecology of Àmveme SJgDdgDq at Middleback, and has two aims. Section É'.1 tests the above prediction, and considers the results in relation to the 'predictability' of the pollinator spectrum. Section 6.2 describes pollinator exclusion experiments which test the hypothesis of Ford gL eL (1979) that insects are potentially effective pollinators of the flowers of Àmvemq (see section 1.3). Page 165 6.7,2 Hethods 6,1.2.1 Timing of anthesis and floral lifespan The temporal pattern in flower opening was monitored in May and Àugrust 1981 and in Àugust 1983. Between t2-t08 inflorescences were labelled with jer¿ellers' tags on 4-8 plants and the number of buds and newly opened flowers recorded every 6 hr for 1.5-3.0 d. To determine floral lifespan, I labelled inflorescences on eight plants in October 1983, and recorded the floral phase (Fig. 1.3) of individual buds and flowers every 1-3 d over 2 ¡,tk. 6.7 .2.2 Breeding system Field observations of pollen loads on Àmyema qugldenq stigmas were made between 0800-1100 hr on 25 June 1982. The number of pollen grains on stigrmas çras scored on a sample of inflorescences on four plants using a 30 x pocket microscope. Flowers which opened duri.ng the observation period were scored prior to visits by animals, because the proximity of the observer deterred birds from feeding near the plants and flying insects and ants were absent. In order to examine the breeding system and timing of stigmatal receptivity, I examined pollen germination on stigmas and pollen tube penetration of styles using fluorescence microscopy after controlled hand potlinations in the field. Four flowering branches were tagged on each of eight large mistletoes in late September 1983. Light terylene voiLe (mesh 0.8 x 0.3 mm) bags were placed over three of the four branches and tied tightl.y to the stems (0.8-1.5 cm in diameter). The bags excluded insects and Iarger animals from flowers. The fabric $ras secured so as not to brush against the inflorescences inside. I labelled open flowers on aII branches periodically. By 79-2t October, flowers belonged to two cohorts, 'old' flowers which had opened 2-10 d previously, and 'young' flowers which were 7-Z d old. one of three treatments sras applied to eech baggêd branch: Page 166 (1) flou¡ers hard-pollinated with self-pollen (to test for compatibility to self-pollination) i (2) flowers hand-pol.Iinated with the pollen of other plants (cross-pollination) ; (3) flowers not hard-pollinated (autogamy). Flowers on the unbagged branch ürere unmanipulated and served as controls. Flowers were hard-pollinated by repeatedly brushing the stigma with one or more fresh anthers until a conspicuous amount of pollen adhered to the stigmatic surface. Flowers which were self-pollinated received pollen from rrewJ.y opened flowers in the bag at the time of pollination. Cross-pollen was obtained from newly opened flowers or Chinese Lantern phase buds on other plants within (short cross) or beyond (Iong cross) a 200 m radius. Most short cross-pollen came from mistletoes within a feç¡ metres of the experimental plants. Flowers collected for cross-poIIen r.rere either used immediately or stored in air-tight glass vials out of the sun for up to 24 hr prior to use. I harvested all flowers 6-22 hr after pollination, inchxling flowers which had opened since pollination and Chinese Lantern phase buds, and fixed them immediately in 3:1 ethanol-acetic acid. In the la-boratory, the styles of five flowers per combination of flol¡er cohort, treatment and plant were excised and softened in 8 H KOH for 3-6 hr. They were prepared for fluorescence microscopy in the manner ctescribed by Vithanage et gL (1980). Under the microscope, I counted the ¡umber of po1len grains on or near the stigmatic tissue, the number of pollen tubes penetrating between the stigmatic papillae, the number penetrating stylar tissue as far as the 'neck' (the narrowest point of the style immediately proximal to the stigma) and the furthest distance down the style penetrated by a pollen tube. The values obtained for replicate styles were pooled to give a mean and proportion for each treatment and plant, and the data were analysed with two-way analyses of variance (treatment by plant, without replicatÍon) using the GENSTAT statistical package. I also recorded the position of the tips of the embryo sacs in squashed preparations of five plants to determine whether young and old flowers Page 767 dÍffered in the deqrree of embryo sac extension in the style (section 1.3). 6.1.2.3 Experiments measuring seed set Further investigations of the breeding system were attempted by measuring the seed set resulting from controlled hand pollinations in two experiments. In March-April 7987, at least four branches in heavy bud were tagged on ten large mistletoes. Each of the three treatments described in the preceding section $ras applied to one branch per plant and the remaÍning branches r¿ere used for controls. In four plants, the autogamy treatment was modified to test for apomixis by emasculating buds which were at least two-thirds grown. Buds were emasculated by removing the bulbous tip of the corolla and developing anthers surrounding the distal style. Treatment branches bore 63 - 311 buds, and the swn of buds on control branches varied between 381 - 1054 per plant. I hard-pollinated flowers, on average, every 5 d (range, 7-!6 d) in the manner described above. In the second experiment, I increased the frequency of hand pollination and minimised the duration of bagging because none of the bagged treatments set many fruit Ín the first experiment. I used the eight plants described in section 6.2.7.2. Treatment branches were bagged j.n late September 1983, after the removal of flowers and young fruit on aII branches. Flowers were hand-pollinated at mean Íntervals of 3 d (range, 1-8 d). Bags $rere removed on 79-27 October and seed set scored on 15-16 November towards the end of flowering, 6.t.2.4 Nectar production Nectar stancìing crops and 24 hr production were measured between 30 Àpril-Z l.fay 1981 and 23-24 June 1982. In 1981, samples of t3-23 flowers were picked from six large flowering mistletoes at dusk and the volume and concentration of nectar in each flower measured with 10 or 25 ¡rI microcapitlary tubes and a 0-50% Stanley & Bellingham hand refractometer. Àt the same time as the samples were picked, terylene voile bags were placed Page 168 over one or more branches on each plant to exclude animals from flowers. Àt dusk the next day, samples of tt-28 flowers were picked from the bags on each plant, and floral nectar content measured. In 1982, samples of 18-30 flowers were picked in the late afternoon from an arbitrary eight plants and the nectar content of individual flowers measured. Àt the same time bags were placed on branches of another eight plants. Samp).es of bagged flowers were picked 24 hr later and their nectar content measwed. Nectar concentrations and volumes were converted to milligrams of sucrose eguivalents, taking into account the density of the sugar solution (Bolten et eI* 7979). 6.1 .2.5 Pollinators I made notes on insect and bird visitation at mistletoe flowers as opporbunit.ies arose during fieldwork. I recorded the foraging behaviour of insects at flowers and the freguency with which they contacted anthers and stignras. Insect abundance at flowers s¡as generally Ioç¡ (r¿ith the exception of lridomyrmex sp., çfp F), and most data were obtained opporLunistically when environmental conditions suited particular taxa. Hoerever, I systematically watched flowers in May 1981 and Àugust 1983, and recorded all jnsects on marked mistletoes along the census traverse on seven occasions. Specimens of taxa visiting flowers were collected and identified. Potential avian pollinators !,ere mistnetted, and their facial feathers, base of the biII and nares sampled for pollen using the glycerine jelty technigue of ltooller et aI- (1983). The equipment was cleaned between sampling individual birds, and control samples were t.aken to check for contamination. gbservations of the frequency of flower visitation by birds were made on 1-2 May 1981. Three large plants were watched in periods spread evenly throughout the day. I timed the length of foraging bouts of birds in the plants and measured their foraging rates on flowers. Throughout the study, I noted all observations of birds feeding at flowers in mistletoe canopies. Page 169 6.1 .3 Results 6.1 .3.1 FIoraI phase In early development, the buds of f,myema quandanq were amanged in 2-rayed umbels of triads. Bud abortion, abiotic damage and herbivores combined to reduce the number of buds in many developing inflorescences prior to ard during flowering, such that the numbers of developing infLorescences with 1-6 buds were approximately equaL across the flowering season (Fig. 6.1). Developing inflorescences of seven or more buds were rare The transition of the mature bud through anthesis to the abscission of petals occurred in five floral phases (Calder et aI. 1979', Bernhardt et gl- 1980; Fig. 1.3) and spanned 6-10 d. Flower opening began with the medial separation of the petals (Chinese Lantern phase btrd). PoIIen was presented as the petal tips separated at anthesis because the anthers dehisced in the mature bud. Newly opened flowers (Male phase) were characterised by the presence of conspicuous yellow pollen in the anthers, minimal reflexion of the petals with anthers arranged closely around the neck of the style (Plate 3), and deep crimson filaments, style and inner surfaces of the corolla. Most pollen was dissimted within hours of opening, after whictr the anthers withered and darkened. The petals reflexed as the flower aged, the stigma increased slightly in size, and the red of the filaments, petals and style faded. These feattrres characterised the Female phase. The MaIe phase generally Lasted 36-48 hr. However, some flowers were identifiably Fema1e within 24 tE while others persisted in MaIe phase for up Lo 72 hr on the tnsis of the morpholgical criteria above. The distance between the stigma and the nectary at the base of the style averaged 28 mm. IndividuaL flowers tended to open at night or during the morning, but not in the afternoon (Ta-ble 6.1). In Àugust 798t, most flowers which opened between 0600-1200 hr did so before 0900 hr. Many inflorescences, particularly those with five or six buds, took several days to open fully. Page 170 The first four flou¡ers opened at a rate of about t daya, the fifth and sixth opening more rapj.dly (Table 6.2). Consequently, at least 45% of. inflorescences passed through a biphasic stage where MaIe and Female phase flowers were borne simultaneously (Table 6.3). 6.1.3.2 Breeding system In the mature bud, the morphological relationship of the anthers to the stigma eras similar to that described by Bernhardt et eL (1980). The stigma was usually pressed agaÍnst a Iayer of petaline trichomes at the tips of the enclosed petals, and the anthers dehisced against the distal style belor¡ the stigma (Fig,6.2). Most flowers observed in the field on 24 June 1982 had pollen adhering to the upper hemisphere of the stigma (Table 6.4). The stigmas of flowers which opened during the 3 hr observation period generally bore pollern, but less than the amount on older flowers. The flowers lrere protandrous. Few 7-2 d o1d flowers had pollen associated with the stigmatic surface in squashed preparations, incJ.uding those which had been hand-pollinated (Table 6.5), and only one young flower rc.6%) had germinated grains adhering to the stigirna. By contrast, polì.en adhered to or occurred adjacent to the stigmatic tÍssue of most 2-10 d old flowers, and most of the stigmas bore germinated pcrllen grains (Tables 6.5 & 6.6). The difference in stigmatic receptivity between young and old flowers r.las correlated with morphological changes in the stigma surf ace. The unicellular stigmatic papillae in young flowers and Chinese Lantern phase buds were small and compactly aranged and the thick cuticular caps of the cells fluoresced brightly (Plates 4 e 5). The papillae of older receptive stigmas were expanded alrd less compactly arranged, with conspicuous intercellular clefts in which pollen grains lodged. The cuticles of older stigmatic papillae fluoresced dimly. Most of the 2-70 d old flowers which did not have pollen adhering to the stigma were unreceptive, judging from stigmatic morphology. Page 777 Amor¡g 2-I0 ð old flowers, there was no significant difference among tr-eatments and controls in the proporbions of stigmas and styles which were pollínated or penetrated by pollen tubes (Table 6.6). Flowers which ç¡ere bagged to exclude pollinators and were not hand-pollinated received pollen through mechanical autogamy. Mechanical autogamy and natural pollÍnation were equally effective in leading to poì.len tube penetration in styles which were not artÍficiatly pollinated. The proportions of stigmas with adherent pollen grains and with pollen Eubes penetrating stígmatic tissue were lower in the autogamy treatment and controls than for the hand-pollinated treatments. The difference approached marginal significance in the latter instance. Hand pollination transferred large and conspicuous amounts of polJ.en to stigmas whereas pollen was rarely visible on the stigmas of control or bagged non-pollinated flowers. Accordingly, among 2-10 d old flowers, hand.-pollinated flowers had significantly gnreater amounts of pollen adhering to the stigma and more pollen tubes penetrating the stigmatic tissue than control and bagged flowers which were not artificially pollinated (Table 6.7>. However, there was no dj.fference among treatments in the number of pollen tubes penetrating the stylar neck or in the furthest distance çrenetrated by polten tubes. Flowers ç¿ere self-compatible and equally receptive to cross- and self-pollen. Bagged flowers which received self- and long and short cross-pollen showed simiLar amounts of pollination and stigmatic and stylar tube penetration (Table 6.7), There was no significant quantitative clifference between autggamous and natural pollination. Control flowers and bagged flowers v¡hich were not hand-pollinated shor¡ed similar amounts of poJ.tination and styLar tube penetration. The embryo sacs in bhe stylar tissue fluoresced dimly (Plate 4) and were generally difficult to locate in squashed preparations. Up to four were found together in styles and, r¿ith one exception, the tips of co-occurring Page 772 embryo sacs were at the same height in the style. In old flowers the embryo sacs generaJ.Iy reached to between 0.5-0.8 of the length of the style (Table 6.8). Those in two young flowers only reached 0.2-0.3 of the way up the style, suggesting that the growth of the embryo sacs in the style continued after anthesis. The furthest distance that a pollen tube penetrated down a style was 0.3 of the stylar length, overlapping the upper limits to which embryo sacs grrev¡ in old styles. Contact between pollen tubes and embryo sacs $ras searched for, but not found. 6.1.3.3 Experiments measuring seed set from hand pollinations In the 1981 experiment, most emasculated buds aborted prior to flowering, particularly buds which u¡ere not fully grown. By June-July, two plants had set negligible seed set inside bags containing a high density of phloem-feeding eurymelíd bugs which bred up in the bags. The branches had incurred a moderate degrree of defoliation. Small numbers of eurymelids occurred in some bags on other plants but the branches had not suffered the same degree of defoliation. Compared to control branches, significantly J.ess flowers on bagged branches had set fruit by June-July, including flowers which were hand-poLlinated (Table 6.9). Consequently, hancl pollinations were terminated. Bags were left in positjon until the end of flowering when all branches were rescored. The bagged branches of the two plants which had been moderately defoliated were entirely defoliated by late September. À moderate degree of leaf abscission had occurred inside bags on a further three plants, and persistent leaves were brittle and less succulerrt than those on unbagged branches. One of the plants did not produce new vegetative growth on bagged branches in late spring, unlike the control branches. In the remaining five plants, seed set resulting from hand pollinations in the first half of the flowering season remained significantly less than that of control branches (Table 6.9). Page 173 In the second experiment in 1983, seed set in aII bagged teatments was sigmificantly lower than on control branches. There was no difference in seed set among bagged flowers which received cross- or self-pollen, and those which were not hand-pollinated (Table 6.9). 6.1.3.4 Nectar production The mean nectar content of unbagged flowers was similar in 1981 and 7982 (Table 6.10). 0n both occasions the sugar content of flowers ranged from about 0-5 mg sugar, with most flowers containing ]ittle or no nectar and a few containing relatively large amounts (Fig. 6.3). Host of the bagged flowers had secreted nectar after 24 l:r, few flowers containing less than 1 mg sr-qar. MaIe phase flowers produced more nectar than Female phase or transitional flowers (Table 6.10), particularly in 1982. The differences in production were reflected in the average standing crop of nectar Ín Male and Female phase flowers (Table 6.10). MaIe floç¡ers contained more nectar than Female phase flowers, particularly in 7982. 6.1.3.5 Pollinators Many species of insects and birds visited the flowers of Amvema quardgnq for pollen or nectar. For convenience, I distinguished four classes of floral visitor: diurnal ftying insects, ants, moths and birds. Diurnal flyir¡g insects Eleven taxa visÍted flowers on more than one occasion (Tab1e 6.11). l,fost ç¡ere recorded in autuinn and spring, only one specÍes visiting flowers in June and three in July. Àlt species visited flowers for nectar, and the bees ard syrphÍd fly also harvested pollen. The taxa occurred in low density, usually as solitary foragers. À11 srere more abundant on sunny days than urder cool or clor:dy cor¡ditions. Most of the taxa in Table 6.11 came into contact with the stigmas and anthers of ÀByema quardanq ard were potential pollinators. However, the Page 174 Iarge megachilid bee, Chaligodoma genlluctuogg, was a more effective potlirntor than the remairder. It was active across most of the day (0800-1700 hr) in spring, persistently visited flowers, visited only a few flowers per plant, ard made large interplant movements. l{hen collectÍng pollen, it hovered above l{ale phase flowers and scooped pollen from the anthers into the abdominal scopa, simultaneously brushing the stigma. It often contacted the stigmas of Female phase flowers when entering the corolla tr¡be to drink nectar. It collected pollen betç¡een mid and late morning, interspersed with visits to flowers for nectar. Nectar foraging predominated later in the day after the pollen in newly opened flowers was dissipated. The remaining taxa in Table 6.11 were less effective polljnators, either because they were infreguent floral visitors (butterflÍes, medium-sized bees, wasps) or $,ere too small to freguently contact the stigma (small colletid ¡"""f./fne smalI bees generally avoided touching the stigma except with their antennae. They also spent long periods ha:rresting pollen on indivÍdual flowers, and made relatively few interBlant movements. Ants Seven species of ant visited Amyema quandgng flowers for nectar on more than one occasion and an individual of an eighth species was collected with pollen adhering to the abdomen (Table 6.tZ). Ànts occurred on misttetoes in all months although individual species exhibited changes in seasonal abundance (Fig. 6.Ð. Taxa also exhibited species-specif ic differences in density. Some were solitary foragers, others congrregated in densities up to 100 planta and lridomyrmex sp. (gp F) occurred in even higher densities in summer when terding eurymelid and scale insects. Ànts were often the most common flora1 visitors. In spot checks of inflorescences thror.rghout the day on l May 1981, Iridomvrmex sp. (gp F) was the only insect four¡d on flowers and occurred on an average of. 78% of. Page 175 inflorescences. It also dominated vísits to flowers during 15 min observation periods on the same day, visiting the distal parts of an average oE 702 of flowers per observation period (Table 6.13). Ànts, principally Crematoqaster sp., srere the main insect visitors to flowers between 16-18 Augrust 1983 (Table 6.14 ) . IridomyEmex sp. (gp F) was the only ant recorded coming into contact with both anthers and stigrmas. 0n 1 l{ay 1981, it contacted anthers, stigmas or distal styles, ard petals or filaments on 28%, 62, and 65v" of. visits to distal parts of flowers, respectively. Species of lridomvrmex were active foragers ard repeatedly traversed the vegetative and floral surfaces of plants which they occupied. Other genera generally avoided the distal parts of flowers. Since Iridomvrmex sp. (gp F) was the only lridomvrmex species which frequently occurred on mistletoes, it was potentíally the most important pollinating species of ant. Moths Several species of moth srere recorded visiting flowers for nectar in autumn ard spring (Table 6.15). Diurnal moths were rare, and only two were recorded. Nocturnal moths rdere generally scarce, both during observation periods ín May 1981 ar¡d Àugrust 1983 (Tables 6.13 & 6.74) and at other times. However, high densities $rere encountered at dusk on the $¡arm still evenings of.26 March, 20 and 21 Àpril 1987, ?tllay 1982 ard 23 August 1983. 0n each of the evenings, moths of several species appeared 20-30 min after sunset in densities of up to 100 per mistletoe canopy. They foraged for nectar at the sides of flowers but the larger species also clambered over the tops of inflorescences and repeatedly contacted anthers and stigmas. The smaller species generally avoided the tops of inflorescences. Birds Nine species of bird foraged at Àmvemg suandanq flowers for nectar (Table 6.16). They probed down the corolla tubes of flowers ar¡d brushed Page t76 anthers ard stigrmas. AII species sampled durir¡g the flowering season bore f quandam pollen on the bÍII or among the facial feathers. PoIIen loads varied from a few grrains on mistletoebirds to tens of thousands on some honeyeaters. The largest pollen loads were recorded in l'fay ard JuIy 1982, Honeyeaters were persístent floral visitors throughout the flowering season (Chapter 5). The flowers of three plants observed on 1-2 May 1981 received an average of about t honeyeater probe daya (Table 6.17). 0f the species in Table 6.16, only the spiny-cheeked and singing honeyeaters $rere resident in the study area and persistent floral visitors. The spiny-cheeked was more abur¡dant than the singing (Àpper¡dix 2) and spent most of its foraging time visiting À- quardenq flowers during the flowering season (section 5.3.2). By sheer weight of numbers, it was the most important avian pollÍnator in the stt¡dy area. 6,7.4 DÍscussion 6.1.4.1 Floral phase The morphological differences between HaIe and Female fl.oral phases in Àmyema quanda¡g srere correlated with the functional attributes of young and old flowers. Pollen dispersal characterised the first day of floral life. Pollen was dissipated wÍthin hours of flower opening due to the activities of birds ard insects. Àt the same time, the stigma of young t-Z d old flowers was not receptÍve to pollen. The position of the embryo sacs low in the style of two young flowers suggested that fertilisatjon was unlikely at this stage, even if pollen tube penetration of the upper style was to occur as in older flowers. Pollen receipt characterised older flowers with spent anthers, and the stigmas of most 2-70 d old flowers were receptive. The stigmas of 30% of the older flowers which did not bear germinated pollen after hand pollination ç¡ere still unreceptive. This observation suggests that the transÍtion to stigmatic receptivity occurs about day 3 ot 4, assuming that flos¡ers srlrvive for an average of I d. Page 177 The changes in stigmatic morphologry accompanying the transition to pollen receptivity were similar to those in protandrous populations of A- miquelii arrd À- miraculosrJ$ (Berr¡hardt & Knox 1983). The structure of the intercellular clefts bet$reen the stigrmatic papillae of receptive stigmas complemented the triradiate morpholoqy of the pollen grrains (Plate 5). Po]len which lodged ard germinated in the clefts was unlikely to be brushed off by the repeated visits of pollinators to flowers. A secondary advantage of the trilobate morphology of the pollerr of most Loranthaceae may be an increase in the probability of grains lodgíng between the feather barbules of avian pollinators (Bernhardt & Calder 1981a). However, specific apperdanges for catching in the barbules and barbicels of feathers are not a prerequisite for the bird dispersal of pollen, judging from the sub-spheroid pollen morphologies of many bird-pollinated taxa (cf. Knox 1984). The l.fiddleback population of Àmvema cruandanq displayed a greater degrree of protandry than the temperate population studied by Bernhardt et aI. (1980). They found that most stÍgrmas of seven HaIe phase flowers hand-pollinated in the laboratory at anthesis bore germinated pollen after 24 hr, and obtained a partial positive response to an esterase test for stigrmatic receptivity. Protandry reduces the chances of autogamy and therefore increases the chances of out-crossing. It is associated with self-incompatibitity among Victorian Àmvema species (Bernhardt 1983b). Thus, compared to ther temperate population, Middleback plants tended towards an outbreeding rather than inbreeding system, contradicting the prediction of the arid zone unpredictability hypothesis. Two factors are probably important in accounting for the greater degrree of outbreeding in the HiddLeback population of Àmvema quandanq. First, l,fiddleback plants have reliable sedentary pollinators in the spiny-cheeked honeyeater and, in lesser densíty, the singing honeyeater. Spiny-cheeked honeyeaters are present throughout the flowering season (no matter when it begins), are persistent floral visitors, and defend Page 178 territorÍes centred on the plants (Chapter 5). Furthermore, f,- quandanq does lo.t not compete with other bird ftowers in the community for pollinatot"/ gy contrast, the pollinator spectrum of the À- quendancr population studied by Bernhardt & Calder (1981a) varied seasonally, and the flowers of À- E¿andanq appeared to attract less birds than a sympatric congener, À- æ¡fuIgg, which flowered simultaneously. Thus, Ín the temperate population, times may occur when there are temporarily few pollinators, and much of the po1len deposited on stigrmas must be L pendulum pollen. SelectÍon ought to have favor.¡red a greater degree of sel.f-fertility in the temperate population than at Middleback in order to maintain a compara-ble level of seed set. The hosts of the two populations also differ markedly (section 3.1.4.3). The temperate population parasitises short-Iived understorey acacias, whereas western myall is both the dominant tree at Middleback and long-Iived. Suitable habitat (host branches) for the temperate populatÍon are probably both more scarce and transitory in time than for the arid zone population. This difference ç¡ould favour the evolution of a greater (short-term) fecundity through self-fertility in the temperate population. 6.1,.4.2 Breeding system Hand pollination oÍ. 2-70 d old flowers increased the number of pollen grrains adhering to the stigma and the number of pollen tubes which penetrated the stigrma. Honever, hand pollination had no effect on the number of tubes which penetrated to the neck of the style, nor in the furthest distance penetrated down the style by a pollen tube. The period of timé permitted for pollen germination and tube penetration after hand pollination G-22 hr) was evidently too brief under f ield conditions to allow a sigrnificant number of tubes to penetrate further than the stigmatic tissues. Much of the pollen tube penetration in the stylar tissue probably resulted from autogany (in bagged flor.rers) ard natural pollination (in control flowers) prior to the hand pollinations. Page 179 Àmyemg quandalq was self-compatible, as far as can be judged from pollen tube penetration of the stigrmatic and stylar tissues. This finding is in agrreement with the results of Bernhardt e! gL (1980) for the temperate population. However, the amount of autogamy in l'liddleback plants contrasted with their laboratory findings. Bernhardt e! eL (1980) allor¡ed an unstated number of ir¡dividually excised, Chinese Lantern phase buds to open on an agar-sucrose mediun. No pollen was found on the stigmas after 24 hr. They argred that the stignna, compressed against the petaline trichome cap in bud, did not come into contact r¡ith anthers during petal separation. The Middleback population was similar in the arrangement of the anthers ard stigma in bud. Nevertheless pollen stas deposited on 80% of stigmas at anthesis and pollen penetrated stÍgmas of 4O% of. the older flowers excluded from pollinators. Flowers opening in the field were buffeted by wind and foliage which could have knocked pollen on to stigmas. By the same mechanism, older flowers in biphasic inflorescences could have been mechanically potlinated with pollen from later opening flowers. Thus, despite general agrreement with Bernhardt et al. (1980), autogamy was potentially more important in contributing to seed set in Middleback plants than their laboratory firdings wouJ.d suggest. 6,7.4.3 Experiments measuring seed se Both attempts to measure the seed set resulting from hand poltination treatments were unsuccessful insofar as the bagged treatment branches set far fewer fruit than controls. Àt the end of the first experiment, I reasoned that two types of factors could have been involved. The bags themselves might have had deleterious effects on one or more processes involved in frr¡it development after fertilisation. Evidence of bag effects included the abnormal abundance of phloern-feeding bugs, which probably had a deleterious effect on the nutrition of the branches on which they occurred, and thus on the chances of fruit set (Stephenson 1981). The Page 180 build-up of nectar in flor¿ers which resulted from the exclusion of pollinators may have led to bacterial or fungal infections damaging to the flowers or yourl¡ fruits. Long-term effects, inch.rding leaf abscission ard inhibition of veEetative growth, could have resulted from a reduction in Iight transmission thror.rgh the bags, or to detrimental changes in microclimate arourd bagged foliage. GrowLh and maintenance processes in bagged branches would have been affected if the cord restricted the flow of phloem or xylem sap. The second set of factors was related to the adequacy of pollination Ín treatments in which I artificially pollinated flowers. Hand pollinations once every 5 d may have been too infreguent or transferred too Iitt1e po1len to achieve a high probability of fertilisation. In the second experiment, the likelihood of long-term bag effects was minimised by restrÍcting bagging to 3 wk. Àt the same time, I increased the frequency of hand pollination and compared the effectiveness of pollination of bagged and unbagged flowers using laboratory techniques. The results, above, showed that hand-pollinated flowers received more pollen than those in the autogramy treatment or controls, ard that levels of poltination and tube penetration in the latter two grroups were similar. Thus the reduced seed set in aII bagging treatments was due to eÍther the lower quality of the zygotes resulting from autogamy and hand pollinations, resulting in the abortion of most shortly after fertilisation, or to deleterious bag effects which came into play within the floral lifespan of the first flowers to open on bagged branches. The low but similar seed set across all treatments in both experiments suggested that the zygotes resulting from autogamy and hand pollinations with self- and cross-pollen erere egually viable. The increase in pollen transfer and tube penetration resultíng from hand pollinations was not reflected in sigrnificantly higher seed set, although pollen germination, tube penetration and seed set in the autogamy treatment were generally Iowest. Page 181 6.7.4.4 Pollinators Most flowers opened at night or in the first few hours after sunrise, ard observations repeatedly shor.¡ed that virtually all pollen was dissipated by early afternoon. Therefore, floral visitors active at night or dr.¡ring the morning s,ere primarily responsible for polIen dispersal. During obsen¡ations of flower opening in 1981 and 1983, the pollen in newly opened flowers accumulated through the night because nocturnal flower visitors (moths and ants) were scarce or absent. Honeyeaters visited flowers from dawn onwards whereas most diurnal insects became active later in the morníng. Honeyeaters bore large pollen loads anong the facial feathers and in the nares, ard were probably responsible for most pollen dispersal. Later in the morning, diurnal flying insects collected or consumed the remaining pollen at flowers which had opened overnight or during the morning. pol]en-collecting bees were probably effective pollinators on days when they were active, partÍcularly the large Chalicodoma semiluctuosa. SmaII ants were often abundant floral visitors in autumn and spring but did not linger on the anthers and stiEnas which they contacted, and never accumulated large pollen loads. In some plants, pollen contact with ant integumentg results in reduced germination and pollen-tube grrowth, probably due to the antibiotics which ants secrete to combat pathogenic microorganisms (Beattie et sL 1984). For these reasons, ants were probably Iess important pollinators of |- quandang than birds and bees. Moths were only abundant flora} visitors occasionally, and at dusk when least pollen was available for dispersal. Nocturnal moths are generally most active at dusk (Proctor & Yeo ti72) due to the usual decline in temperature betu¡een dusk and dawn. l'foths probably dispersed little pollen compared to birds and bees. MaIe phase flowers produced more nectar and had larger standing crops than older flowers. Bernhardt & Ca1der (1981a) fourd a similar pattern of nectar production in Anvema ouandanq in Victoria. Birds and insects often Page 182 discriminate between the morphologÍcal floral phases Ín certain plants, biasing visits to the phase containing the most nectar (Gottsberger 7977; Paton 1982c; D.C. Paton & B. Lamont, pers. comm.). Foraging honeyeaters probably biased their visits to the MaIe phase flou¡ers of A^ quandancr in the expectation of a grreater nectar reward. The likely result of the pattern of nectar pnoduction, then, was to increase the rate at which pollen was removed from the anthers of newly opened flowers and dispersed by pollinators. Several of the smaller bee species and the syrphid fly were comparatively ineffectual pollinators, but on fine days harvested a considerable amount of pollen at newly opened flowers. À^ quandanq may have evolved the strategy of maximising nectar production in newly opened flowers to increase the likelihood of pollen dispersal by birds in the early morning prior to the activity period of the small pollen-harvesting insects. Colletid and megachilid bees nectared at Female phase flowers although such flowers had less nectar than young flowers. The corolla expansion accompanying flower ageing afforded insects easier access to the nectar of older flowers. The abundance of insect visitors at Àmyema suandanq flowers varied seasonally. Most species ¡rere recorded in autumn and spring but very few visited flowers in June and JuIy, presumably due to the inhibitive effect of low winter temperatures (Fig. 2.4) on insect activity. The large megachíIid bee was only recorded in sprÍng. The freguency of flower visitation by insects also varied fron day to day, deperdirg on environmental conditÍons. Insects were less common at flowers on cold days and were therefore less reliable pollinators than homeothermic birds which foraged every day throughout the daylight hours. Page 183 6.2 POLLINÀTOR EXCLUSION EXPERIMENTS 6.2.7 Introduction I Ford et eI- (7979) hypothesised that the open flowers of Amvemg may be pollinated by insects should bird pollinators fail to visit flowers (section 1.3). I tested the hypothesis that insects could contribute to the seed set of ¡- quandanq flowers by excluding dÍfferent size classes of pollinators from the flowers of Àmyema quandaDq in the 1981 ard 1982 flowering seasons. The predictions of the hypothesis $tere that (1) seed set would be maximal on branches exposed to aII pollinators including honeyeaters, and (2) an appreciable number of flowers exposed to insects but not birds would also set fruit. In retrospect, the unexpected occurrence of autogamy in the breeding system of Àmyema zugJtéEnq (cf. Bernhardt et aI- 1980; Bernhardt 1983b) complicated the interpretation of results. Seed set in the a.bsence of birds might have resulted from autogamy rather than insect pollination. However, Ínitial observations made durÍng the 1980 flowering season permitted the predictions to be refined. Insect visitation at flowers $tas markedly reduced in winter. If insect pollínation contributed to the seed crop of plants, the seed set on branches caged from honeyeaters but accessible to insects rras expected to be lower in winter than in autumn or spring, reLative to controls. 6.2.2 Methods I used wire cages to exclude pollinators from flowers in two consecutive flowering seasons. At the start of the flowering season in 1981, 13 large mistletoes in treavy bud were selected, including four plants which were used in the hand pollination experiment (section 6.1.2.3). Each plant received the following treatments: (1) one branch enclosed in a terylene voÍIe bag (autogamy); (2) one branch enclosed Ín a wire mesh cage (hexagonal mesh, average length of side 1 cm); and, (3) one branch caged wjth wÍre rnesh (hexagonal mesh, average lengbh of side 2 cm). An additional 1-5 branches Page 184 were tagged as controls. One-centimetre mesh excluded all birds from flowers 'a (except for a few flor¡ers within 1-2 cm of the cage edge) but permitted access to insects. Ànts, small colletid bees and noctuid moths (body lengrbh, 20 mm) readily passed through the mesh to forage at flowers. Two-centimetre mesh excluded honeyeaters from flowers (except for a few of the flor.¡ers within 5 cm of the cage wall), but permitted access to small birds and insects. Histletoebird droppings were found inside some 2 cm mesh cages demonstrating that small birds entered the cages. Treatment branches bore 80 - 635 buds, and the total number of control buds varied from 215 - 1054 per plant. Àbout a third of the branches had begun flowering, so the few flowers and young fn¡it present were removed. Àt the end of each plant's flowering season (September or November), I counted the number of young fn¡it on all branches. In late 1981, 14 large mistletoes with abundant deveLoping fruit (from flowerÍng in 1981) were selected to monitor dissipation of the fruit crop (section 7.7>. These plants received the same treatments as above, and seed set across the 1982 flowering season $tas measured. However, two branches were tagged for bagging, and the hag was alternated between branches over successÍve sampling intervals to minimise possible effects associated with extended bagging. In non-bagging periods, these branches Í¡ere exposed to all poltinators. Data for the two branches from bagging intenrals were pooled for the autogany treatment. Data from non-bagging intervals were used to examine the effects of intermittent bagging on the seed set of flowers exposed to all pollinators. In both 1981 and 1982, I monitored flower turnover and seed set on experimental plants at intervals across the flowering season. In 1981, I counted the nunber of brds, flowers and young fruit on the branches of nine plants aL 7-2 mo intervals, and of all plants aL 2.0-2.5 mo intenrals in 7982. À small dob of enamel paint about 1 mm in diameter was applied to the s¡nall persistent bract at the base of the gynoecium or on the peduncle of Page 185 newly set fruÍts. Coloured paints were used to differentÍate the fruit set in each sampling inten¡al. In 1982, buds, flowers and young fruit which had been danaged or destroyed by the lan¡ae of herbivorous moths were counted separately from ungnazed floral units. Seed set ratios ar¡d an herbivore predation index were calculated for each treatment and plant. Data for the control branches were pooled to give a single value per plant. Cumulative seed set across the flowering season was calculated as the nunber of accumulated young fruit expressed as a proportion of the original number of buds. Total seed set was the number of young fn¡it at the end of the flowering season, expressed as a proportion of the original number of buds. Flower turnover was calculated as the sum of buds and flowers at the beginnirg of a sampling interval minus the sum of buds and flowers at the end of the intenral. Instantaneous seed set was defined as the amount of yor-rng fruit remaining on a branch one interval after the sampling interval in which it was set, expressed as a proportion of the f lower tr.¡rr¡over for the interval. Final seed set was the amount of young fruit which had set in a given interval and which remained at the end of the flowering season, expressed as a proportion of the flower turnover for the Ínterval. The herbivore index was calculated as the ratio of buds ard flowers damaged by moth larvae at the end of a sampling interval to the nunber of floral units turned over during the interval. In calculating the mean instantaneous and final seed set and the mean herbivore predation Índex of plants, observations based on a flower turnover (n) of less than 20 were omitted because of the increased error associated with =*ull n.'fy' 6.2.3 Results The experimental plants in 1981 flowered between l'farch and October, and those in 1982 flowered between Àpril and 0ctober. The flowering curve of the floriferous individuals in 1981 was skewed, with peak flowering early in the season, gradually tapering off across the winter and spring (Fig. 6.5a). Page 186 Flower turnover reflected this pattern, and was similar in all treatments a (Fig. 6.6). Flowering in 1982 was not so skewed, peaking in winter-spring (Fig. 6.7a). Large numbers of floç¡ers turned over in each of the main sampling intervals in at¡tumn, winter and spring, but the pooled data for flos¡er turnover r.ras more variable amonçt treatments than in 1981 (Fig. 6.8). Control flowers exposed to all pollinators including honeyeaters set the most fnlit Ín both 1981 and 1982 (Table 6.18). The exclusion of honeyeaters $rith 2 cm mesh and the exclusion of honeyeaters and smaller birds with 1 cm mesh reduced seed set to a simÍlar degnee in each year. The reduction in seed set averaged 21"2" of control in 1981 and 44% in 1982. As in the breedÍrg system work, the autogamy (bagged) treatment set few fruit, seed set being about 75% of. control in both years. In 1982, the flowers exposed to aII potlinators between periods of bagging set less total fruit than controls, but a similar amount to the two caging treatments. The seasonal pattern of accumulation of young fruits in 1981 and 7982 díf.fsred in two main respects (Figs 6.5b and 6.7b). Seed set of the floriferous indÍviduals was higher in 1981, and the accumulation of young fruit on plants peaked later in 1982 due to later flowering. However the seasonal patterns were simÍIar to the extent that young fruit accumulated on control and caged branches at the same rate until early Àugust, when the seed set of control flowers registered an increase over caged flowers. The increased seed set of control branches $¡as maintained across the remainder of the flowering seasons. In 1981 the instantaneous seed set of control and caged branches was sinilar in each sampling Ínterval except JuIy, when caged flowers set a reduced proportion of fruit (Fig. 6.9a). Seed set inside cages was little more than that inside bags in JuIy. In 1982, the instantaneous seed set of caged and control branches $ras again similar in autumn (Fig. 6.10a). Caged flowers set a reduced proportion of fruits in June ard July. In the spring intenral, instantaneous seed set in the 2 cm mesh treatment increased to Page 787 that of the controls, but the value for the 1 cm mesh treatment remained low and was similar to the seed set inside bags. The disparity in instantaneous seed set between control and caged flowers in JuIy 1981 and June-July 1982 was presenred at the end of the flowerirg season in the final seed sets (Figs 6.9b & 6.10b). In 1981, the final seed set of controls was consistently higher across the earlier sampling intervals as well. Thus the ratio of seed set in cages to controls averaged 0.8 across the autumn, dropped to 0.5 in JuIy and increased to about 1.0 in the final spring interval (Fig. 6.9c), In7982, seed set in the 2 cm mesh treatment exhibited a similar seasonal pattern, but seed set in the 1 cm mesh treatment remained low in the final spring interval (Fig. 6.10c ) . Àlthough the instantaneous seed set of control flowers was greatest at peak flowering in both 1981 ard 7982, final seed set tended to increase across the flowering season with only a minor peak in each year coincident with peah flowering (Figs 6.9 & 6.10). Seed set in the autogamy treatment showed a similar increase across the flowering season. Predation of young fruits by moth larvae was noted on several experimental plants in 1981, but the level of damage was not quantified. In one small-mesh cage, total seed set was only 4% because most young fruit were eaten. This case sras exceptional in the magnitude of the fruit loss to herbivores. In 1982 predation of young fruit was negligÍble throughout the flowering season, and confined to control branches (0.2"t" of young fruit damaged). However, predation of buds and flowers by oecophorid moth larvae $ras nore substantial, most damage occr-tming in June and JuIy (Fig. 6.11a), The herbivore predation indices for the caging treatments and controls were similar in the autumn and spring sampling intenrals but herbivore damage was gneater on the control branches in r¡inter (Fig. 6.11b). Thus, herbivore danage inside cages in winter was either similar to or less than grazing Iosses in autr¡nn or sprír¡g, relative to controls (Fig. 6.11c). Page 188 6 .2,4 Discussion The caging experiments in both flowering seasons supported the predictions that bird pollination effected maximum seed set in Àmvema çredg!ÉI, ard that insect pollination $ras potentially effective in contributing to seed set. The exclusion of birds from flowers (1 cm mesh treatment) Ied to reductions in seed set, but these insect-visited flowers stilt set 60-80% of the amount of fruit as controls. The similar seed set in the 1 cm and 2 cm mesh treatments indicated that pollination by small birds (thornbitls and mistletoebirds) and by honeyeaters probing some flowers at the edge of the 2 cm mesh cages had a negligible effect. The 1 cm and 2 cm mesh treatments were effectively the same treatment, permitting insect visitation at flowers but excluding honeyeaters. Insect pollination rather than autogamy $tas responsible for at least some seed set inside cages because the amount of fruit set inside cages consistently declined in the winter months when insect activity was reduced. The autogamy treatment did not show this trend. In 1981, the reduced seed set inside cages was confined to JuIy, whereas in 1982 a similar reduction sras recorded in the interval spanning both June and July. In 1981, the mean daily minimum in June was lrarmer than July, and similar to August. However ín 7982, both June and JuIy were colder than May or Àugust (Fig. 6.72). The amount of insect activity in June may have differed between years due to the differences in temperature. The seasonaL pattern in seed set inside cages relative to controls was similar in both years, except that seed set in the 1 cm mesh treatment in spring 1982 did not increase from the winter level. One can infer from Figures 6.9c and 6.10c that insect pollination was potentially responsible for at least 20-30% of seed set in autumn and spring. However, whether insects actually contributed to the fertilisation of control flowers was not ascertained. The high seed set inside cages in spring, at least in the 2 cm mesh treatment, may have been due to the appearance of Chalicodoma Page 189 semi luctuosa. The loss of most of the newly set fruit to moth lan¡ae in a 1 cm mesh cage in 1981 raised the question of whether herbivores inflicted gireater losses of fruit inside cages in the absence of bird predation, particularly in mid winter when the larvae $rere most abundant. If so, the winter reduction in seed set inside cages might have been an artefact of greater herbivory rather than the consequence of reduced pollinator activity. ln 7982, herbivore damage to young fruit was negligible and confined to control branches. However, the grrazing of buds and flowers by oecophorid moth larvae was more substantial and also peaked in winter. The grazing losses were largest on control branches, thus the relative reduction in seed set in cages was not due to differential grrazing. The grounds on which the experimental plants were chosen differed in the two years. Plants with large bud crops were selected in 1981 whereas plants with large immature fruit crops were used in the following year, many of the developing fruit persisting across the 1982 flowering season. Environmental conditions had also deteriorated to a marked extent in 1982. Both factors qrere expected to influence patterns of seed set in the sane way. Mistletoes suffering a mÍnor to moderate degrree of water stress and with a relatively large persistent fruit crop probably had less resources to allocate to flowering in 1982 than the floriferous individuals in 1981. Peak flowering was early in 1981 and total seed set was higher across all treatments. These differences probably resulted from the postulated disparity in resources available to plants for flowering. The intermittent bagging of branches in 1982 led to a sigmifÍcant reduction (302.) in the seed set of flowers exposed to poJ.linators during non-bagging intervals. Thus, bags deleteriously affected seed set in a way which was divorced from the intended effect of excluding pollinators from flowers, and confirmed the presence of a 'bag effect'. The autogamy treatment set a small percentage of fruit in both years. although the amount Page 190 was presumably reduced due to the bag effect. Seed set inside bags consistently increased across the flowering season. The efficiency of autogamy as a mode of pollination leading to fertilisation was unlikely to have increased as flower turnover declined late in the flowering season. Nor could differential grazing losses be invoked because noth larvae were either excluded from the young fruit (1981) or had a negligible impact (1982). The probable explanation lay in differential patterns of zygote ard embryo abortion operating across the flowering season. Embryos resulting from autogamy may have been initially aborted but retaÍned later in the season. The trend in increasing final seed set was reflected across all treatments, so a decrease in the proportion of embryos aborted may have been a general trend exhibited by plants as flowering progressed. The relatively high seed set inside cages late in both flowering seasons may have been partly attributable to this pattern. Page 191 Table 6.1 The percentage of Àmyema ggandenq flowers opening at different times of the day dr.rring three obsenration periods. Time of May Àugrust Àugust day 1 981 1981 1 983 Àverage (hr) 1 800-0000 52 10 31 31 0000-0600 40 28 24 31 0600-1 200 0 54 38 31 1 200-1 800 8 I 7 I Tab1e 6.2 Synchrony in flower opening in 78 inflorescences observed over 4 d in Àugust 1983. Nunbers of flowers observed to open are shown in parentheses. Rank order Percentage Mean time taken of flower opening to open since in opening synchronously Iast flower (d) 7 31 (58) 2 56 (48) 1.0 (46) 3 58 (31) 1.2 (32) 4 53 (15) 1.2 (18) 5 58 (12) .7 (11) 6 80 (s) .4 (4) Table 6.3 Minimum estimate of the percentage of varying sized inflorescences which passed through a biphasic stage in August 1983, Observations $tere made over 4 d and subsequently at day 7. Consequently, more of the inflorescences may have been biphasic than çrere recorded. No. of flowers/ No. of Hinimum percentage infLorescence inflorescences biphasic 2 77 27 3 15 47 4 76 31 5 18 56 6 18 56 Page 792 Table 6.4 The proportion of flowers with pollen on the stigrma ard the number of pollen grains per stigma, for flowers sampled between 0800-1100 hr, 24 June 1,982. The upper value is the proportion of stigmas which bore pollen, ar¡d the lower data are the mean number of grrains per stigma t S.E. Number of flowers sampled is shown in parentheses. Floral phase Plant 7 2 3 4 Just opened .80 (10) 1.0 (6) .75 (2) .75 ( 4) .7!.5 6.2 ! 7.9 s.8 I 3.0 3.8 I 2.5 Male .33 (18) 7.0 (24) .95 (20) .77 (26) .8 t.3 23.8 I 3.0 22.0 + 4.6 12 .5 + 3.3 FemaIe 92 (26) .96 (27) .84 (19) .74 (23) 4.5 t .7 31 .8 t 4.1 14.6 + 2.9 71.0 ! 2.4 Petal Shed .43 ( 7 ) 1.0 (9) .91 (11) 1.0 (17) 1.0 t 6 34.6 ! 2t .9 75.4 ! 4.t 33.1 t 5.9 Tab1e 6.5 The proportion of stignas with adhering pollen and the number of grrains per stigma in squashed preparations of varying aged flowers of Amvema suandaDg. Flower cohort Flower Proportion of No. of pollen Sample and treatment êge stigrmas with gnains/stigma size (d) adhering pollen X t S.E. Chinese Lantern not .19 1.0 + .6 27 phase bud open Newly opened 0-1 0 0 t9 flowers Bagged & Y hand-po1 1 inated ' 7-2 .06 2 + t 78 o u Autogamy ft .04 t t t 25 n g Control .04 .1 1 1 27 0Id AII 2-70 70 27 .5 + 3,2 185 treatments b 'Includes both self- and cross-pollinated flowers. b Includes control fLowers. Ta-ble 6.6 degnees The proportion of styles of. 2-70 d old flowers with pollen adhering to the stigrma ard showing varyÍng of pollen tr-rbe penetiation. None of the means in eacir row differed at P f .05 using the least significant difference (Sokal ard Rohlf 1981) after analyses of variance of the angufar transformed data. Means ard 95% confidence intervals are back transformed. The original data and anova tables are given in Appendix 3.1. Treatment Variable Cross-pol I inated SeIf- Autogamy Control F ratio' long short pollinated (d.f . = 4,26) Number of plants 8 7 8 7 I PoIIen gnains .8 .9 .8 .6 ,6 1.645 NS adhering/adjacent .6 - 1.0 .7 - 1.0 .6 - 1.0 .4 -'.9 .4 - .8 to stígnatic tissueù Pollen tubes .7 .7 7 .3 .5 2.685 NS penetrating .5-.9 .5 -.9 5 9 7 - .6 .2-.7 stigmatic tissue Pollen tubes .4 3 .4 2 .3 .478 NS reachirq stylar .2-.7 t .6 .7-.7 0 5 .t - .6 neck Pollen tubes 4 .3 .3 2 .3 .285 NS penetrating further .t-.7 .1 - .6 .1 - .6 0 .5 .1 6 than stylar neck .o o rA o tl 2.74 \o 'Ec¡=t+ø= (lower (¡J r DatJarã ttre mean (upper value) ard 95 7. confidence inten¡al range). Table 6.7 The number of pollen g"rains ard pollen tubes showing various degrrees of adherence to or penetration of Àmvemg letters were sJerdq,g stigmäs-ã"¿ étii"" in z-10 d old flowers. ú".ns in each row followed by different superscript different at p I .05 using the least sigmificant difference (Sokal and Rohlf 1981) after analyses of variance of the log translormed data. Means and 95% confidence intervals are back transformed. The original data and anova tables are given in Àppendix 3.1. Treatment Variable Cross-pol I irnted SeIf- Autogamy Control F ratiot lorg short pollinated (d.f . = 4,26) Nunber of plants I 7 8 7 I b Pollen grains 23.5 ' 27 .2' 34.2' 6.8 b 6.5 6,158** adherirg/adjacent 72.3 - 44.3 13.7 - 53.3 18.1 - 63. 9 3.t - 14.7 3.0 - 12.8 to stigrnatic tissue2 b PoIIen tubes 15.1 ' 18.3 ' 77 .5' 7.7 b 4.8 7.689tt** penetrating 7 .5 - 29.7 8.7 - 37 .5 8.7 - 34.4 0.4 - 4.4 2.0 - 10.0 stignatic tissue Pollen tubes 2.0 1.5 2.0 0.7 2.0 .959 NS reachingr stylar 0.8 - 4.1 0.4 - 3.3 0.8 - 4.1 0 - 2.0 0.8 - 4.0 neck Furthest distance 0.4 0.4 9.7 0.4 0.9 .825 NS penetrated by a 0 - 1.0 0 - 1.0 0.2 - 7.4 0 - 1.0 0.4 - 1.7 pollen tuber "Uo t (o E. -o 71a,¿ = 2.74 o 2 Data are the mean (upper value) and 952. confidence interval (lower range). 3 Distance $ras measured in stigma ler¡gbhs. Þ\o Page 195 Table 6.8 position of the embryo sacs in the styles of 5 plants of Àmvema quandang. Position of the embryo sac tips Plant No. of styles as a fraction of styJ.ar length' No. 01d Young 0td Young flowers flowers flowers flowers X (range) 7 5 0.7 (.6 - .8) 2 3 0.6 (.5 - .8) a 3 7t L 0.6 (.5 - .8) 9.2 (.2 - .3) 4 7 0.7 5 t 0.4 . Since co-occuring embryo s€rcs generally reached the same height in styles, means were calculated using 1 value per style. Table 6.9 Seed set (proportion of flowers setting fruit) in the 1981 and 1983 hard pottination eiperiments. l'teans in each column followed by a.diffelel!- õ;Ë;i;l iãtt"t differed at P-l .05 usins the least sisnificant difference asãkái unä nohlf 1981) after anãlises of variance of the angrular transformed data. Heans and 952 confidence intervals are back transformed. Sample sizes are indicated in parentheses. The original data and anova tables are given in Àppendix 3.2. Seed sett Treatment 1 981 1983 June-July September . Long .09 . .06 .t7. .05 -.13 (8) .03 - .10 (5) .08 - .29 (7) Cross-poI I inated Short ,07' .04 . .13. .04 - .11 (8) .01 -.08 (5) .05 - .25 (7) SeIf-poIl Ínated .08 . .04 ' .27. .05 - .13 (8) .01 - .08 (5) .77 - .33 (8) . . Àutogamy .05 .11 .01 - .11 (4) .04 - .27 (8) Control .61 b .52b .60 ù .53 - .68 (8) .44 - .61 (5) .47 - .73 <8) F ratio 59 . 1 8*** 60.23x** 11 . 16*r+* (d.f,) ( 4 ,12> (3,72) (4,26) (lower rData are the mean (upper value) ard 952 confidence interval range). Page 196 Table 6.10 The standing crop and 24 hr productivity of nectar for Àmveme quandang flowers. Flowers were sampled at dusk (1981) or late afternoon Q982). The mean + S.E. is shown for all flowers pooled. The mean standing crops of Male, intermediate and Female phase flowers followed by a different superscript letter differed at P S .05 using the least significant difference (Sokal and Rohlf 1981 ), after analyses of variance of the square root transformed data. l.leans and 952. confidence intervals are back transformed. E ratios = 3.42x and 31.18*** on 2,188 and 7,787 d.f . for 1981 and 1982, respectively. Sample sizes are shown in parentheses. The original data and anova tables are given in Àppendix 3.3. Fl.oral phase Nectar content of Productivity flowers (¡rS sugar flowera) (¡rs suSar flowera d{ ) tïgL Male r .59. .43 - .78 (57> 1 .45 Intermediate 2 .54. d .38 - .73 (53) .98 FemaIe .34d .24 - .47 (81) 1.22 AII flowerss .65 t .05 (192) 7,77 1982 ÌlaIe .92. .77 - t.tz (68) 7.32 FemaIe .29d .27 - .40 (127) .57 Àll f lowers 3 .77 ! .07 (97) .87 rData are the mean and 95% confidence interval (sample sÍze) for floral nectar contents. 2 Intermediate flowers were late Male or early Female with small amounts of pollen in the anthers. I Includes Chinese Lantern phase buds. Table 6.11 study. Dir-rrnt flyi¡g insects recorded visiting Àmyema quandanq flor¡ers on nore than one occasion drrirg the Frequency of Seasonal Contact Body visitation to occurrence s¡ith Harvest Taxa (À) length funyema anthers pol lerr ( ¡ron ) quandanq or canopies JFH ÀHJ JÀS OND stigma (S) terf I iesb Lycaenidae: À,s IheçLineslheg g- serDentata 6-8 Infreguent xx xx (Herrich-Schaffer) Oqr¡ris amarvllis meridional is 13-14 Frequent xxx xx xxx À,s Bethune-Boker Hoverfl¡ Syrphidae: + (e) Simosvrphus g4¡d¡CgElis llacq 8-9 Fregr¡ent xxx À Beeg' À + (e) Unknoçn taxon À 7l Infrequent xx xx x Unknonn taxon B 7l Rare x Hegachi I idae: + (c) Chalicodoma semiluctuosa Smith 20 Frequent xx xxx À,s Col letidae: (c) d 4-6 Frequent x xxx xx xx À,s + C-allomelitta spp + (e) Euryglossinae sPP 4.5-5 5 Frequent xx xxx x À,S lfaspsd Scol i idae : Camwomeris !g94gD¡e!9¡g Saussure 28 Rare x x À,s . e: insect Íngested pollen while positioned on anthers; c: insect scooped pollen into scope. ard transported it betueen flowers. Þ Butterflies were identified by l,lr Robert Fisher. Royal S0ciety of south Àustralia. voucher specimens were Iodqed çith the South ÀustralÍan Huseum. specimens l4S-"d t'¡ith the -o . To-xa identified by Dr Eric Hatthews. South Àuetralian l'Íuseun. Hoverfly ard wasp o voucher specimens of all bee taxa except unknow¡ B were collected ard dornted to the ta south Àustralian l{useum. o llestern Àustralian Huseum. d Àt least 4 morphologically ancl behaviourally similar species were involved. tJ {\o Table 6.12 pollen adhering to Ànts which visited the flowers of Àmyema suêdgrrl on more than one occasÍon or were collected with the body. Freguency of Seasonal Tended Drank Contacted UsuaI (À) Body visitatÍon to occurrence Behaviour homopterans floraI anthers abrr:rdance Taxa' per Length Àmvema on nectar or (mm) quardarìg mistletoes b stignas (S) plant' canopies JFH ÀHJ JÀS OND Freguent xxx xxx xxx xxx Àctive e,sc + À,s sLnmer:3-{ Iridomyfnex sp. 2.5-3 winter:1-2 (sp F) Iridonvrmex (pr¡rpureus gp) 6.5-7.5 Infrequent xx x Àctive e + 2 'blue'sp. Cre¡natoqaster sp. 3.5 Frequent xx xx xxx x Sluggish e,sc + À 2 + 7 Camponotus sp. 7 Freguent x xxx xx xx Àctive sc (ephippir,¡rn gp) + 1 Camponotug 6-6.5 Infrequent xx x Àctive ? mggeqereuc pollen 1 Camponotus 10 Rare x x Àctive e adhering gouldianug to abdomen + 1 Calomvrmex sp 8-9 Frequent xx xx xx xx Àctive e + t PodSryEmq 6 Infreguent x xx xx x Sluggish e edelqi-dei -o o footnote on Page 52 ao b'See e, eurymelids; sc, scalei nsects. ll . ( 3, 101 -1000; 4, >1001 \D 1, 7O: 2, 11-100; æ Page 199 Table 6 . 13 Number of insect visits to 200 Amvemq cruandgng flowers obsen¡ed in 15 min periods on 1 May 1981. Only visits to distal parts of flowers $¡ere scored for lridomyq[ex sp. (gp F). tl.r., number not recorded. Time of day (hr) Insect Taxon 0905 1100 1310 1520 1810 2055 (dusk) lrrdsnymex sp. (gp F) 37 9 7 7 27 n.r. n Bee, unknown taxon À 2 :' Callomclitte sp. Hoth : 7 7 Ta-ble 6 . 14 Number of Ínsect visits to lmygma çlJandang flowers on eight plants between 16-18 August 1983. Visits were recorded in t hr periods at four times of the day over 48 hr. Time of day (hr) Insect Taxon 0000 0700 t2g0 1 800 Çregatggqsler sp. 4 2 Unidentified ants ! 7 Euryglossinae bees 2 Callomelitte sp. I 2 Caflomeliltq sp. 2 7 Çhalieodome semilugtussa ; Singgyrchus grendiqornis 2 _ Moth spp. ¿ Page 200 Ta-ble 6.15 Hoths col.lected while visiting flowers of Amvemg EJendg¡q for nectar. Taxa' Body Collection date and time Iength (mm) Diurnal species ÀgaristÍdae: Comqe.tug þebrr (Àngas) 24 28 September 1983, 1650 hr Oecophoridae: Unknown sp. I 28 September 1983, tt20 lE Nocturnal species Noctuidae: Àqrotig nundg tialker 76-20 23 Àugust 1983, 1815 hr 24 August 1983, 0845 hr Qþ4¿godeixis eEçIcnlifera t7 23 Àugust 1983, 1815-1900 hr ( Guenee ) Amphipyrinae sp. t 13-14 23 August 1983, 1815-1900 hr Àmphipyrinae sp. 2 77 23 Àugust 1983, 1815-1900 hr piatgnes marmarinopa 15 23 August 1983, 1815-1900 hr ( Heynick ) Propatria mundioides 75-17 20 Àpril 1981, 1830 hr (Lower) 1 May 1987, 1930 hr Rlctonis psEqçIypEe 77 20 April 1981, 1830 hr (Lower) 1 Hay 1981, 1930 hr Unknown sp. 7 15 20 Àpril 7981, 1830 hr 1 l{ay 1981, 1930 hr Unknown sp. 2 13 20 Àpril 7981, 1830 hr Pyral idae: Etiella sp. 11-13 28 September 1981, 1815-1900 hr Phycitinae spp 5-10 28 September 1981, 1815-1900 hr LoxoEteqe affinitalis t7 28 September 1981, 1815-1900 hr (Lederer) Phyatinae sp. 28 September 1981, 1815-1900 hr Geometridae: ? Semiothrsq sp. 9 26 Ì'larch 1981, 1930 hr . Specimens of aII taxa were identified by llr Ted Edwards, CSIRO Division of Entomology, and Dr Eric Ì'latthews, South Australian Huseum. Voucher material was lodged with their respective institutions. Table 6,16 grains samples from species observed foragirrg at sucld=als flowers for nectar, and the number of pollen in Bird Ànycma obtained from mistnetted birds. The numbãr or porr"n g.ãin" *u" counted in three traverses of the pollen sample slide each bird. Status Frequency Number of À- E¡e¡QelS pollen grains per birdó Bird in of nectar X (¡) ard range spec i es' study foraging at area¡ À- quandanq' Dec80 Feb81 Nov81 Jan82 üar82 Hay82 JuI82 Sep82 Nov82 t716(1) Inlard thornbill R 0 Chestnut-rumped R 0 thornbi L l 8088( 1 ) Red wattlebird L P 2059(10) 533(10) 779(1) Spiny-cheeked R P 0(4) 0(5) 32(5) 0(1) 4096(1 ) 3243(7) 77-947 honeyeater 2-722 768-13084 262-6803 YeI Ior¿-throated L P miner 1916(3) 352(7 ) Singing R P 0(1) 1(1) 3733(2) honeyeater 2809-4656 206-5156 45-87 4 7787(1) YeI low-plumed v P honeyeater fJhite-fronted N P honeyeater 759(2) 35(2) 7ß) l'listletoebird R 0 64-253 30-39 2-15 Ð YelJ.ow-plumed honeyeater Liqhenostomgs ornqtus. q .scientific names in Àppendix 2 except for the o oñ, nomad; N, regional nomad; V, vagrant. These terms are defined in Àpperdix 2' resident; L, Iocal Nr '0, occasional; P, Persistent. O d 10 control slides scored 0 pollen grains each. Page 202 Table 6.17 gbservations of honeyeater foraging on a total of 1440 flowers on three Àmyeme qUetdeng plants , 7-2 May 1981. 1 May 2 MaY Time spent foraging on 1 636 2159 f lor¡ers by birds' (s) Ratio of daylight hours to 2.276 7.200 time spent watching flowers Foraging rateb (probes sr) 0. 413 0.415 Estimate of number of 1 538 7075 flov¡ers visited d{ . Spiny-cheeked honeyeaters, singing honeyeaters and yellow-throated miners accounted f.or 74%,17% and 9% of. bird foraging, respectively. There was no significant difference in their foraging rates, so the data for aII species were pooled. b Foraging rates calculated from 661 and 1209 s of honeyeater foraging tine on 1 and 2 May, resPectivelY. Table 6.18 Total seed set in lBvema ggandenq pollinator exclusion experiments in 1981 and 1982. Means in each column followed by the same superscrÍpt letter are not significantly different at P < .05 using the least significant difference (Sokal and Rohlf 1981) after anaJ.ysis of variance of the anguJ.ar transformed data. Means and 95% confidence intervals are backed transformed. The number of plants are shown in parentheses. Original data and the anova table are given in Àppendix 3.4. Seed set Treatment 1981 1982 . Control .44 .26 " .37 - .51 (13) .79 - .35 (14) 2 cm Mesh .32b .15b .26 - .40 (11) .08 - .23 (10) 1 cm ilesh .31 b .09 b .25 - .39 (11) .05 - .16 (13) Àutogamy .05 . .03 . .02 - .09 (11) .00 - .07 (tt) Intermittent pol J. inator .t4b exposure/bagging .07 - .22 (t0) F ratio (d-f. ) 40. 47**tf ( 3,30 ) 9.36*** ( 4, 40 ) .25 .15 March May August oz fUJ a uJ lrfr 0 j 24 6 I 10 2468 uJ fE NO. OF BUDS/INFLORESCENCE October o 2 4 6 8 10 2 4 6 fr- 'ul ='lOJJI l!I elrL -l 2or MA MJJASON MONTH Fig. 6.7. The number of developing inflorescences with 1-11 buds remaining season, expressed as frequencies 'ú at different stages of the 7982 flowering Þ of the original number of inflorescences in Harch. Buds and floç¡ers were 'cl (see o counted on 14 plants section 6.2.2.) ¡\) O G) Page 204 Tri a stg Ptl t\ t I An ì' I l stv \., I I I F¡I Fig. 6.2. Longitudirnl section of the tip of the mature bud of lmvemg zugndq¡g. The stigma (Stg) is wedged against the Ínside surface of the tips of the unseparated petals (PtI). The anthers (An) are forced against the style (Sty). The stigmatic surface presses against a dense layer of petaline trichomes (Tri). Filament, FiI. Page 205 0.5 h) tmm&g[-u*horo- -E_ r-n (b) oz ut of *H kdÄn -,k-E--'r l¡J E t! 0 (c) tr 5 t¡J CE, 0 [-u[ln.r[l -r --I o.3 (d) 1 male at 6.72 0 Ln*L[.L l-n-!-!_E¡-e¡- 0 1 2 3 4 5 FLORAL SUGAR CO|,¡TENT (mg /flower) Fig. 6.3. Frequency distributions of the sugar content of nectar in Àmvema q,ránd.!g floweis in May 1981 (a a b) and June 7982 k & d). (a & c) Standing õõp in unbagged flowers at dusk (1981) or late afternoon (982)l (b & d)_ accümulated ãectar Ín bagged flowers after 24 hr. Male phase (open); Female phase (black), and flowers intermediate between Male and Female phase (defined in Table 6.701 stipple bars). Page 206 0.6 (a) A o.3 o a-----a\ o ^ O- z 0 a ft¡J a o.2 (b) frLIJ IL o O uJ 0 l- o.2 (c) IJJ o É. o ¿^ A ^----{-- o.2 (d) .a 0 n.î. n.r n.1. SEP. NOV APR. DEC. FEB.. MAR. MAY JUL. 80 80 81 82 83 83 83 83 DATE Fig. 6.4. The proportion of marked Amvemg cruandg¡g plants on which ants of (a) Iridomyruet sp. (gp F), (b) Camponotug sp. (ephipnium gp), (c) CaloEyrmex sp., ard (d) Crematoqasteg sp. occur¡ed along the 3.3 km tiaverse. Total frequency (O); ants terding eurymelids (A); ants drinking nectar at flowers (O). n.r., species abundance not recorded. Page 207 a z (a) fr 1 uJ o =J 0 lJ. 6 (b) t- L¡J CN o 3 uJ l.U U) 0 MAM JJ ASON 1 981 Fig. 6,5. Seasonal pattern in (a) the number of flowers per branch and (b) cumulative seed set in Anyema quandanq in 1981. Data are the mean + S.E. for I or 9 plants. Controls (tr); 2 crn mesh (O) ; 1 cm mesh (Â), and autogamy treatment (V). Flowering data are expressed as proportions of the original nr-¡mber of buds. Page 208 .o1 (a) 0 .01 o (b) zF- J fL 0 o z .01 ul f (c) ø ul fE II j tU 0 fr .01 (d) 0 MAM JJ ASON 1981 Fig. 6.6. Freguency distributions of the proportion of flowers turned over on marked branches of 9 Àmyema quandang plants in 1981. Distributions are shown for control branches (a), branches caged with 2 cm mesh (b) and 1 cm mesh (c), ar¡d bagged branches (d). Area of the bars is proportional to turnover Ín flowers. Page 209 CI 7 É 0.1 (a) ¡,u =o J 0 tL 0.5 (b) þ UJ ct) o tU ul cf) 0 M AM JJ ASON 1 982 Fig. 6.7. Seasonal pattern in (a) the nunber of flowers per branch and (b) cumulative seed set in Àmyema quandang in 1982. Data are the means I S.E. for 13 or 74 pJ.ants. Flowering data are expressed as proportions of the original number of buds. Controls (tr); 2 cm mesh (O); 1 cm mesh (A); autogamy ( v), and intermittent exposure to poll.inators ( v ). Page 210 .oo6 (a) .006 (b) o t- z .oo6 J fL (c) zo f,lrJ o t! É. II .oo6 t¡l (d) fr 0 006 (e) o MAM JJ ASON 1 982 Fig. 6.8. Freguency distrÍbutions of the proportions of flowers turned over on marked branches of. t4 Amyena quandanq in 1982. (a) Controls; (b) 2 cm mesh; (c) 1 cm mesh; (d) autogamy; and (e) intermittent exposure to pollinators arìd bagging. Àrea of the bars is proportional to flower turnover. IJ o la FINAL SEED SET o RATIOS ÊN) FINAL SEED SET INSTANTANEOUS CAcES:CONTROL SEED SET t¡b o C'l o (rl Þ C- If.! (o o) C- @ io Ø o o C' z g) a Fig. 6.10 U)l 5 o (a) t l- ztUr.l 4u) lo I ÍH $a z 0 t- UJ 5 U) (b) o uJ ttJ U) J z tr o L1.OU) 3E (c) F-z ¡.u o Øç¡ fi !,;, a 3 5 ão z MAM ASON TL JJ 1 982 Figs 6.9 & 6.10. Seasonal variation in (a) instantaneous seed set, (b) final seed set and (c) the ratio of final seed set in each caged treatment to that of controls in Amvema qggndenq. SymboJ.s as Ín Fig 6,7. Fig. 6.9: data are the means 1 S.E. of 5-9 plants in 1981. Fig.6.10: data are the means 1 S.E. of. 4-74 plants in 1982. The black and white bars on the x-axis indicate the mean sampling inlervals. Page 2t2 U) tU ØÉ. e o.o dã (a) oüLL rr 9:a- 'r- öHO \J*k ,^r 0 cE ;'iÌ fLË È .o8 (b) d .o4 T 0 J o É. fLz (c) Io 1.1 F-o i'9 7 F I.IJ ru= 3 trkF¡ MAMJ ul JASON fE 1 982 Fig. 6.77. Seasonal variation in (a) the proportion of the original number of buds eaten by herbivores, (b) herbivore predation index (HPI, see text) and (c) treatment HPI relative to controls. Data are the means + S.E. of 4-14 plants. Symbols as in Fig.6.7. Page 213 20 la \ >ï- Whyalla 2ur 5 =5tr<\-þ 15 \ ãH Nonning z> <. < r.u ruF o MAMJJASON MONTH Fig. 6.12. l{ean daily minimum temperatures for l{hyalla and Nonning station ttÓO m north-west of Hiddleback) in 1981 (+) and 1982 ç{-). Data from Commonwealth Bureau of Ìleteorology. CHÀPTER 7 FRUITING DISPLÀY, INFECTION REQUiREMENTS, ÀND SEED DISPERSÀL 7 ,7 FRUITING DISPLÀY 7.1.1 Introduction The fruiting displ.ays of plants are a compromise between (1) the desirability of concentrating reproductive effort when the abiotic environment is most suita-ble for fruit maturation, (2) maximising the exploitation of seed dispersers, arrd (3) minimÍsing losses of fruits and seeds to predators. Selection pressures on the timing of other components in the life cycle, such as flowering time, germination and establishment may also necessitate adjusLments in fruiting schedule (Levin 1978>. Considerable evidence points to the importance of seed dispersers and predators as selection agents which have moulded the fruiting strategies of temperate and tropical plants dispersed by vertebrates (Snow 1965; Janzen !969, 1977: Thompson & ltillson 7979; Stiles 1980, t9821 Fleming 1987; l{ilLson & Thompson t982; Knight & Siegfried 1983; Herrera 1984a). The adaptive significance of the fruiting displays of Àustralian mistletoes has not been studied in detail. Reid (1985) noted a tendency for sympatric species to fruit at different times of the year in both temperate and arid South Australia, and similar patterns are evídent elsewhere in Australia (Keast 1958; Blakers et eI- 1984). Staggered fruiting seasons suggest that the species concerned may have competed for the services of seed dispersers in the past (Snoç¡ 1965). Chapter 4 described the fruiting patterns of a large number of individual Àmvems quandang, and Chapter 5 established that, at most, only two species of resident frugivore, the spiny-cheeked honeyeater and mistletoebird, were important dispersal aqents. In this chapter, I further consider the factors which may have influenced the evolutÍon of the fruiting Page 215 display of À- qgen$g¡q. In the remainder of this section, I report details of ripe fruit production, removal by frugivores, and the impact of seed predators on the fruit crop. Sections 7.2 ard 7.3 consider the seasonal ¡ntterns in seed germination, hypocotyl growbh, postdispersal seed predation and establishment. Section 7.3 also reports work which elucidated the types of host branches which A- quandang seedlings could infect. The final section compares the seed dispersal of the spiny-cheeked honeyeater and mistletoebird in the light of the infection requirements of seedLings. 7 .7.2 Hethods I monitored the abundance and dissipation of Àmvema quqndang fruit by counting the number of ímmature, ripe and predated fruit on marked branches of nine plants at irregular intervals between April 1981 and February 1983. Six successive cohorts of fruit set during flowering in 1981 were marked with different coloured enamel paints (section 6.2.2). The dissipation of fruit set in each cohort was recorded during the subsequent fruiting season. Most branches were bagged between January and March t982 Lo provide seeds for infection experiments (section 7.3), Control branches were not manipulated at any other time. I also measured the abundance of ripe fruit and epicarp bases and the removal of ripe fruit on the 14 plants described in section 6.2.2. between October 1981 and November !982. The position of the bag on marked branches was alternated at each reading, erxposing ripe fruits on the previously bagged branch. I returned 24 hr later and recorded the number of fruit which had been consumed by birds. 7 ,1.3 Results 7 .7 .3.1 The ripe fruit The ripe fruits of ÀEygmq qUgldeng were ellipsoid, measuring 7-13 mm in length (Plate 3). Each contained one seed consisting of a chlorophyLlous embryo largely embedded in a white endosperm (Fig. 7.7), Seeds occasionally contained two or tlree embryos. Ttre dispersal unit or 'seed' comprised the Page 276 true seed, which lacked a testa, and the adherent endocarp and mesocarp, The mesocarp was differentÍated into an inner opague mucilaginous tissue called viscin (Lamont 1983; Salle 1983) and a thin outer zone of clear watery tissue. Passage of the seeds through the digestive tract of the spiny-cheeked honeyeater or mistletoebird, or a brief period of sucking, r.emoved the sweet-tasl-ing outer zone of the mesocarp and part of the inner mucilaginous tissue. Large immature fruits $tere grey-green and the same colour as the foliage. Às the fruit matured, it swelled and passed through a green-ripe phase. Fruits were often talçen by birds when green-ripe, particularly when the starding crop of ripe fruit was low. If not removed, green-ripe fruits c:ontinued to swell and the epicerrp turned dull yellow. ÍJhen the standing crop of ripe fruit was large, most ripe fruit on plants was yellow-ripe. At such times, a small proportion of ripe fruits over-ripened on plants and were eventually abscised. Over-ripe fruits were characterised by a deepening of the colour of the epicarp from yellow to yellow-brown, and a loss of turgor in the mesocarp and epicarp through dehydration. Seeds adhered to substrates by virbue of the viscid mesocarp. Sereds from yellow-ripe fruit had a more succulent mesocarp than those from green-ripe fruit. The adherence of such seeds was improved by removal of the outer portion of watery and mucilaginous tissues, resulting in the production of an elastic viscin thread attached to the seed stalk. Seeds adhered to substrates by virtue of the remaining mesocarp surrounding the sreed and the viscid tlread. Viscin drjed within minutes or hours, depending on ambient conditions. However, it retained the capacity to reabsorb water for some days, reswelling upon wetting. 7.1.3.2 Ripe fruit production and removal The annual fruiting seasons of the nine marked plants merged in successive years between October and December (Fi1.7.2), as described for Par¿e 277 the larger sample of plants along the traverse (section 4.3.1.3). Ripe fruj.t from the 1981 and 1982 fruiting seasons were simuLtaneously available among the plants in early November 1981. Similarly, ripe fruit from the 1982 and 1983 seasons were simultaneously available in December 1982. The young fruit crop was largest towards the end of flowering in both years, declining marginally prior to the production of the first ripe fruit. The rate of crop dissipation was highest early in the 1982 fruiting season (Fig. 7.3). Thereafter the size of the crop declined more slowly. SÍmilar trends were evident in the latter part of the 1981 fruiting season and the early part of the 1983 season (Fig. 7.2). The rapid production of ripe fnrit early in the season resulted in large standing crops of ripe fruit by January 1982 (Figs 7.4, 7.5 & 4.2). The standing crcrp of ripe fruit inside bags had increased by early March (FÍ9. 7.4) despite the decline in fruit turnover. Birds could not remove fruit from bags. Ripe fruit probably persisted on branches in an edible form for a fortnight or more, and thus tended to accumulate inside bags. 0n unbagged branches, the standing crop of ripe fruit declined after January (FÍgs 7.5 & 4.2) due to reduced production, the removal of fruíts by birds and, to a minor extent, the destruction of fruits by herbivores (see below). Ripe fruit and basal epicarp remains always comprised a mínor fraction of the total crop of fruits (Fig. 7.2), indicating that mature fruits were produced at a relatively loç¡ rate across the season. The amount of fruit set at different stages of the 1981 flowering season was positively correlated with the intensity of flowering (Fig. 7,6), despite the fact that. final seed set increased across the flowering season (section 6,2.T. Fruit tended to ripen in the sequence in which it was set (Fig. 7.7), Most of the fruit set in March-Àpril ripened 8 mo later at the beginning of the fruiting season, while the fruit set in October did not ripen for a subsequenL 7t-72 no. Ttlere were, however, extreme instances of fruit set late in the flowering season which ripened only 5 mo later, and Page 218 fruit set early in flowering which ripened up to 18 mo later. The sequential dissimtion of fruit of varying ages was reflected in the composition of the standing crop of ripe fruit across the fruiting season (Fig. 7,4). Figure 7.7 indicates that fruit in the last two cohorb,s was dissipated both shortly after fruit set and late in the fruiting season, 10 mo later. The early peak in fruit dissipation sras not due to fruit maturatÍon and removal but to abortion of some of the young fruits during early development. The number of fresh epicarp bases of ripe fruit (see section 4.2.t) were four times more numerous on branches in summer than winter (Fig. 7.5a), jndicating that frugivore populations ccrnsumed more ripe fruit in summer. The short-term likelihood of ripe fruit being consumed uras measured in removal experiments (Fig. 7.5b). Almost aII ripe fruit on previousJ.y bagged branches was removed within 24 hr of exposure to frugivores in November 1981, when ripe fruit on plants eras scarce. Two months later when rapid fruit production had produced a maximal standing crop, virtually no fruit r¿ere taken after 24 hr, The rate of fruit removal was al.so low across the flowering season ín winter 7982, but increased as the standing crop of ripe fruit declined towards nil at the end of the fruiting season. 7 .7.3.3 Seed predation The seeds in immature and ripe fruit were predated by three main agents, the tephritÍd fruit fly Cerapitella loqen'Lhi (Froggatt), moth larvae of the pyralid subfamily Phycitinae, and pJ.atycercid pamots (blue bonnet Ngrthiella hgematoqaster and Port Lincoln ringneck ÞernarÈius zonarius). The fruit fIy oviposited in developing fruits. The maggot which hatched in the seed ate the embryo and endosperm, causing premature yellowing of the cpicarp. Fruit contajning a large maggot. were spongey to Louch and thin, and were mostly left intact on plants by birds. Pyralid moth larvae ate a small hole in the epicar¡r of a developing or ripe fruit and remained inside the fruit until the contents were consumed, Ieaving the epicarp an empty shell. Page 2!9 Frass was deposited outside the epicarp around the entry hole. One grub often predated several fruits on an infructescence. Parrots removed immature or ripe fruits irrdividually, split the epicarp between the mandibles, and ate the embryo and endosperm. Their activities were distinguishabl.e from Iegitimate frugivores because parrots removed most or all of the fruit, leaving only the peduncle and a tiny section of basal. epicarp attached to the plant. The remains of split epicarps and adherent viscin and endocarp were invariably found beneath the plants in ç,hich parrots fed. Predispersal seed predators generally inflicted small losses on the fruit crop (Table 7.1). However, in November 1982, 7I"¿ of the remaining developing and ripe fruits of the 1982 season stere predated. This was at a time when the young fruits of the 1983 crop were still small in size, and seed predators biased their attentions to the few remaining large fruits of the previous season. ÀIthough emus ate ripe and immature fruit in summer' (section 5.3.1 ) and some branches which $rere regularly counted were less than 2.1 m above the grround, I found no evidence of the removal of fruit from marked plants by emus. 7 .t.4 Discussion 'J'he annual pattern in rÍpe fruit prcrduction of Àmyema suandans was more or less correlated with the consumptíon pressure exerted on the ripe fruit crop by frugivorous birds. Epicarp bases on marked branches s,ere more abundant in summer when spiny-cheeked honeyeaters fed on the fruit than in winter when the small population of mistletoebirds constituted the sol.e consumers. However, the correlation between production and consumption was not precise because both the standing crop and t.he removal rate of ripe fruit varied markedly in a period of high fruit production and consumption between November 1981 and January 1982. The sequential ripening of the fruit crop in the order in which Page 220 fruits were set sr-rygested that the apportionment of resources for fruit nraturation e¡as under the physiologÍcal control of parent plants. Solbrig (1980) speculated that natural selection might favour autocratic physiological mechanisms in developing embryos which diverted a disproportionate amount of maternal resources to themselves at the expense of other embryos. However, in the case of ÀBvema guandans, seeds ripened in a predetermined non-random manner, indicating that the maternal control of resource aLlocation to seeds was stronger than the embryos' individual abilities to attract resourceg. In plants in which resources are available for fruit maturation year-round and where certain production patterns are advantageous to the extent that they meet the needs of seed vectors, strong nnternal control of fruit maturation has probably been evolutionarily important. l.foth larvae, fnrit flies and parrots are well knowrr seed predators of a diversity of plant taxa in various parts of the world (Janzen 197t), Despite the continuous availability of a crop of immature and ripe fruit on plants, predispersal seed predation was relatively minor. Reid (1985) argued that two characteristics of Àmyeme ouandanq had evolved to reduce ¡rr:edispersal seed predation. First, although many lorarrthaceous and viscaceous mistletoes have thin, semi-translucent epicarps (Lamont 1983), the epicarp of f qua¡danq is thick. Despite the fact that fruit persist on the plant for many months in an immature state, the mesocarp differentiates Iate in fruit development prior to maturation. The thickness of the undifferentiated pericarp may dissuade fruit flies from ovipositing in Ímmature fruit and moth larvae from eating through tissues to reach the developing seed. Second, unlike the archetypal bird-dispersed fruit, the ripe fruits of À- qJandang are cryptically coloured, initially grey-green ond later duLl yellow. Visually orienting seed predators sruch as pa.rrots and emus must inspect a plant at close quarters before determining the size of its fruit crop, arrd are Likely to miss some fruits, even when stationed at Page 22I the canopy. 0n the other hand, sedentary fnrgivores such as spiny-cheeked honeyeaters and mistletoebirds which are dependent on the fn¡it take more time to search plants for fruit than generalist seed predators such as parrots and probebly learn the position of fruiting plants. 7.2 GERHINÀTION AND HYPOCOTYL GROI¡TH 7.2.7 Introduction Anyema quandanq fn¡ited year-round in an arid environment with large seasonal differences in a¡nbient conditions. This section examines whether the seeds germinated and gnew in all seasons, and whether a brief period of sucking affected seedling survíval compared to unsucked seeds. I also compared the survival and grrowth of seeds defaecated by spiny-cheeked honeyeaters and mistletoebirds. 7 .2.2 l'fethods observations of the seeds of ripe fruit indicated that the hypocotyl protruded from the endosperm into the mesocarp to varying degrrees, and up to 1 mm past the distal endocarp. Accordingly, I defined germination as the extension of the hypocotyl more than 1 mm past the surrounding endocarp. To deterrnine whether the seeds germinated within intact fruit, I compared the Ier¡gth of the h¡pocotyl in seeds from over-ripe fruit with those from ripe fn¡it. I compared the sunrival and growth of sucked and unsucked seedlings between November 1981 and 0ctober 7982. Seeds were excised from ripe fruit in 1 cm mesh cages on 14 marked plants. Àbout half the seeds were sucked briefly to remove excess viscin, and both the sucked and unsucked seeds were placed in labelled plastÍc petri dishes. In November 1981 and the first half of January 7982, the dishes srere placed on a gravel bench in a shadehouse at the l,tiddleback Fietd Centre, and the seeds allowed to germinate. Due to the rapid death of seedlings in early January, dishes were subsequently Page 222 transferred to a 1 cm mesh tray 0.5 m above the gravel. I suspected the seedlings died quickly because of the high temperatwes at the gravel surface during the day. In late January, the survival and growth of seedlings srere compared on the grravel in the shadehouse and in an adjacent barn. The barn lacked walls, so temperatures in the full shade of the barn roof were lower than those in the shadehouse. Between 20-24 seeds were picked from each of five plants and the seeds apportioned equally between two myall branches and two dishes. One stick and a dish were placed in the shadehouse and the other stick and dish were placed in the barn. During fieldwork between November 1981 and October 1982, I collected A$vemq quandanr seeds defaecated by spiny-cheeked honeyeaters and mistletoebirds, and placed them in petri dishes in the shadehouse. Seeds defaecated by the two species were allowed to grrow for similar periods in each month. However, due to differences in collection dates, the average period of gnowth of seedlings defaecated by spiny-cheeked honeyeaters $tas slightly longer than for mistletoebirds. t{hen hypocotyl grrowth in most seedlings was advanced but prior to substantial seedling death or loss of vigour, I recorded the color-r and length of the hypocotyls. Hypocotyl length was measured between the distal endocarp and hypocotyl tip. Hypocotyls were classified on the basis of colow as healthy (pea g'reen), dying (dull or dark gneen), or dead (bro$rn or black). À fer¡ embryos lacked chlorophyll and were r¿hite, yellow or pink. Hlryocotyls which were dying, non-chlorophyllous, or had not germinated were collectively termed moribund. 7 .2.3 Results Seeds germinated inside the epicarps of over-ripe fruit, and the hypocotyl often grew the length of the seed within the intact fruif. The epicarp and mesocarp in over-ripe fn¡it began to dry out prior to abscission. Host of the seeds from ripe fruits germinated in the shadehouse in Page 223 November 1981 ard between Harch and October L982 (Table 7,2). The hypocotyls grrew in various directions and rarely forrned holdfasts (see section 7.3) against the dish or adjacent seeds. Hypocotyls attained lengths up to 16 mm in 27-40 d grou¡bh. However, their shapes vrere usually convoluted, so actual Ier¡gths $tere greater than the linear spans recorded. Virtually all seeds deployed during the first half of January were dead or dying after 14 d (Table 7.2). In the experiment in the latter half of January, all seeds had died on the grravel in the shadehouse after 16 d (Table 7.3). À significant proportion survived and grew in the adjacent barn at lower temperatures and reduced tight intensity. There was no significant difference in seedling survival between those on sticks and in dishes in either place (Table 7.3). Most of the bird-defaecated seeds deployed above the gnavel in the shadehouse during the same period germinated and grew, The sucking of seeds had no sigrnificant effect on the proportion whÍch died or ç¡ere moribund in any month (Table 7.2), However, removal of the outer mesocarp by sucking significantly enhanced the lengttrs which hypocotyls attained in March and August. Sucking had no effect on hypocotyl lengLh in other months. The proportion of seeds which died or were moribund was consistently higher amorìg seeds passed by spiny-cheeked honeyeaters than mistletoebirds (Table 7 .Ð. However, the difference was only sigrnificant in November 1981. The average length of the hypocotyl in seedlings defaecated by mistletoebirds was consistently gneater than for spiny-cheeked honeyeaters but, again, the difference e¡as only significant in November 1981. The experiments monitoring the survival and growth of seedlings in the shadehouse were not designed to statistically compare the viability of bird-defaecated seeds with those obtained directly from plants. However, comparison of the hlpocotyl lengths of defaecated seeds with those from plants collected about the same time suggested that bird ingestion had Iittte or no effect on hypocotyl growth (cf . Tables 7.2 e,7.4), Horeover, Page 224 any effects appeared to be variable in outcome. In March 1982, sucked seeds were pennÍtted to grrow for a shorter time than seeds defaecated by mistletoebÍrds, but produced longer hypocotyls. In May 7982, the converse was true. Sìeasonal conditions were most favourable for seedling survival and growth in autumn and spring. Mortality was highest in January after only short periods of growth, even when petri dishes were placed up off the grravel (Table 7.Ð. The proportion of infirm seedlings was loç¡est between March-May and August-Seplember (Tables 7,2 & 7.4). In the nolr-summer months, the hypocotyl growth of seedlings defaecated by mistletoebirds was more rapid in Àpril and November than in winter (Table 7.4). 7 .2.4 Discussion Removal of the seed from the epicarp generally breaks the predispersal dormancy of mistletoe embryos (Lamont 1983). The epicarp is strongly cutinised and lacks stomates or pores in Àmvema preissii and Huellerina celastroides (Mcluckie 1923; Lamont 1983). A high internal concentration of COz resulting from respiration Ín the young fn¡it is sufficient to prevent germination untÍI the epicarp is n¡ptured in f preissii (Lamont 1983). À símilar explanation probably accounted for the inhibition of hypocotyl growbh in the intact ripe fruit of [- quandgnq. Upon over-ripening, the epicarp became pervious to gaseous exchange because both the epicarp and mesocarp dried out. Seeds presumably germinated in over-ripe fruits because the internal C02 concentration fell below the level which inhibited germination. Itespite the seasonal fluctuations in ambient condÍtions, a majority of seeds germinated and grew at all times of the year. The only exception was the first half of January when seeds in the shadehouse died rapidly. The shadehouse/barn experiment indicated that the higher temperatures or light intensity at the giravel surface in the shadehouse were lethal to seedlings. Page 225 Since a majority of the bird-defaecated seeds placed above the gravel germinated and girew during the latter half of January, the temperature at the qrravel surface appeared to be the main cause of seedling death. Seeds defaecated by birds in autunrn and spring suffered less mortality and had higher growth rates than seeds defaecated in summer and winter, respectively. The intermediate temperatures in autumn and spring were probably optimal for seedling survival and growth, as they are for Amye$a preissii in the warm-temperate semi-arid zone of south-western Australia (Lamont 1983). À- preissii has a germination range of 40-400C and an optimum range for elongation of 250-300C. À brief suck to improve the viscidity of seeds did not have a detrimental effect, on seedling survival or growth. Indeed the hypocotyl growth of sucked seeds was enhanced in March and Àugust. Sucking simulated the passage of the seed through the digestive tract of birds to the extent that the outer mesocarp nas removed and a viscin thread formed. There are no previous data to indicate Èhat mrtial removal of the viscid flesh of mistletoe seeds enhances hypocotyl growLh, although the popular misconception that mistletoe seeds dispersed by birds wiIJ. only germinate after ingestion by birds has been disproved repeatedly (Liddy 1983; SaIIe 1983; Lamont 1983; this study). The fact that the positive effect of sucking on hypocotyl growth was only evident in autumn and spring is intriguing. Equally interesting was the seasonal reversal in the relative growth of seeds defaecated by mistletoebirds and those picked directly from plants. Clearly, the physiological role of the mesocarp in relation to seedling growth in the free-living phase requires more attention. Two hypotheses may account for the higher survival and growth rates of seeds defaecated by mistletoebirds compared to spiny-cheeked honeyeaters. First, mistletoe seeds may be damaged during passage through the gut of birds (Liddy 1983; Lamont 1983). This may be caused by (1) the grinding of the muscular gizzardl (2) excessive removal of the mesocarp rendering the Page 226 erdosperm susceptible to desiccation after defaecation; or (3) the effects of the digestive juices on the hypocotyl and endosperm. The specialised gut of the mistletoebird (section t.4.7) enables seeds to be moved rapidly through the digestive tract (Keast 1958). Spiny-cheeked honeyeaters probably have a less specialised digestive anatomy and take Ionger to pass mistletoe seeds. Occasional seeds passed by honeyeaters lacked most of the mesocarp, suggestirrg a long retention time in the digestive tract. Such seeds grew poorly. The second hypothesis is that, because honeyeaters are the }arger and more generalist frugivore, they may be less discriminatory in the seeds which they consume, eating seeds from unripe or damaged fruits as well as ripe ones. Individual mistletoebirds, with a smaller requirement for sêeds, can be more selective and choose fruits with a nutritious mesocarp (and which presumably contain a fully formed seed), and still satisfy their requirements. Àccordíngly, one would expect reduced survival and vigour of seedlings after defaecation by spiny-cheeked honeyeaters. If the quality of the fruit selected by the two species varied significantly, the difference would probably have been most marked in November 1981 when ripe fruit was scarce. The validity of these hypotheses can only be adequately resolved in aviary experiments where both species are fed seeds randomly drawn from a sample of ripe fruits, the retention period of seeds in the digestive tracts of the birds are measured, and the growth rates of defaecated seeds are compared under uniform conditions. Page 227 7.3 INFECTION AND ESTÀBLISTI}IENT OF AUYEMA OUÀNDÀNE SEEDLINGS 7.3.L IntroductÍon Àt least one infection requirement of stem-parasitic mistletoes is precise: seeds have to be dispersed to the live branches of a compatible host species (Davidar 1983b). However, little attention has been given to defining accurately the size and bark characteristics of branches which can be infected. In order to compare the role of different birds in the seed dispersal of Àrnygma quandanq, I determined the kinds of ç¡estern myall branches r¡hich were suitable for seedling establishment. Simul.taneously, I examined the seasonal pattern in seedling mortality in the free-Iiving phase. The aim was to determine what factors were most important in contributing to seedling mortality, and in what seasons establishment was highest. 7 .3.2 Methods The maximum duration of the survival of seedlings in the free-living phase was determined in an experiment in late March 1983. I picked 62 seeds from plants along the 3.3 km traverse and deployed the seeds on dead twigs. The twigs ú¡ere secured Ín fuII shade, and the survival of the seeds and seedlings monitored at 1 mo intervals until all had ¿i.A.t2'/ gver nine occasions between February 1981 and May 1983, I deployed a total of. 26t Àmyeme quandanq seeds on more than 20 western myalls. Seeds $rere removed from grreen- and yellow-ripe fruit on mistletoes and transferred immediately to a nearby tagged host branch. Seeds which were overtly parasÍtised by a Cerapitelfg lorenthi lan¡a or l.rere otheruise damaged were discarded. Many seeds from yellow-ripe fruit did not readily adhere to stems because of the succulence of the mesocarp, so the seed was rubbed gently along the stem or sucked briefly to remove excess flesh and to produce a viscin thread. Seeds were applied irdividually at points along a branch and a map drawn of their positions. Seeds were usually orientated with the seed Page 228 stalk upwards, resembling the orientation of seeds defaecated by mistletoebirds (section 7.4,3.1). The diameter of the stem immediately proximal to the seed was measured with vernier callipers. The colour and degnee of fissuring of the bark on which a third of the seeds were deployed was also recorded. I returned and recorded which seedlings survived some time between 6-18 mo after deployment. The fate of deployed seeds was studied in more detail in experiments betç¡een September 1982 and Àugust 1983. In September 7982, I deployed an average of. 26 seeds on a marked branch of 10 arbitrarily chosen western myalls. Between December 1982 and August 1983, I picked 1-3 seeds from each marked plant along the traverse which bore ripe fruit dr.ring flower and fruit censuses, ard deployed the seeds on a nearby tagged branch of a western myall. I deployed seeds on stems less than 17 mm in diameter and tended to select stems with feç¡ or no fissures in the bark, because observations and the earlier experiments had indicated that seedlings did not establish on thick branches with rough bark. I measured the stem diameter and recorded the bark characteristics associated with deployed seeds, ar¡d returned at 1-4 mo intervals to monitor their fate, Seeds which failed to germinate after 6 mo and seedlings in which the hypocotyl or holdfast turned from grreen to brown or black were recorded as dead. Insect frass in place of seed or seedling remains Lras taken to denote herbivore predation. 7 .3.3 Results The meristematic tip of the hypocotyl generally gnew towards the stem upon whÍch it was planted. The swollen tip of the hypocotyl contacted the stem within days or weeks, depending upon the season, and formed a hemispherical club or holdfast against the bark (Plate 6). An íntrusive wedge of mistletoe tissue penetrated the host periderm beneath the holdfast and, after some months, Iocalised swelling of the host stem was noticeable Paqe 229 around the holdfast. Seedlings persisted as a holdfast for many months prior to the production of leaves or aerial shoots. One seedling produced two small leaves at the shoot apex after only 5 mo. However, most seedlings had not produced leaves after 18 mo. During this period, the cotyledons embedded in the remains of the seed atrophied and were generally abscised, Ieaving the holdfast attached to the stem with a sma1l portion of hypocotyl terminating at the shoot apex. Occasionatly the withered seed remained attached to the hypocotyl (Plate 6). After 24-30 mo, most seedlings had produced an aerial shoot which emanated from the holdfast. Some seedlings produced an additional shoot emanating from the endophytic system whích ruptured through thin stems on the side opposite the holdfast. Most seedlings which grew from the seeds deployed on shaded dead twigs were dead after 5 mo, and all had died at 6 mo. Seasonal conditions between Harch and September were more benign for seedling survival than any other 6 mo period (section 7.2). Hence, I adopted the criterion that a seedling had established when it persisted for 6 mo on a host stem. The bark characteristics of livir¡g western myall stems varied with stem girth. The primary stems were !-2 mm in diameter, smooth, and yellow or brown (Table 7.Ð. Bark produced secondarily was smooth and grey on thin stems. t{ith increasing girth, the bark developed fissures and cracks. Almost all stems gneater than 16 mm in diameter had rough fibrous bark with deep fissures. From 808 seeds deployed between February 1981 and August 1983 on a range of western myall stems, seedlings only established on stems between 1-16 mm in diameter (Table 7.5). Establishment was híghest on smooth grey stems, 3-6 mm in diameter. No seedlings established on branches with moderate or highly fissured bark. Because the proportion of stems with fissured bark increased above 6 mm diameter, establishment percentages declined as stem girth increased between 6-16 mm. Àbout 7Oz. of. seeds established as a result of the deployment of Page 230 seeds between September 1982 and February 1983, prior to the breaking of the drought (Table 7.O. Establishment of seedlings increased to 45-50% after the drought. The higher mortality of seeds and seedlings prior to March 1983 was due varÍously to increased seedling deaths in the holdfast phase (September and December), weak growth of the hypocotyl resulting in seedling death prior to holdfast formation (September to February), or to the failure of seeds to germinate (December and February). The frequency of seedling death in the holdfast phase increased with stem diameter (Fig. 7.8a). other mortality factors either showed no or only a weak seasonal bias. An average of 10% of deployed seeds disappeared by unknown means. Strong wirds dislodged seeds while the mesocarp çras stiII moist, shortly after deployment. This was exacerbated by rain in the days after deployment, which led to reswelling of the viscin. À proportíon of the seeds which disappeared were probably either accidentally dislodged by birds or eaten by herbivores arìd the remains and frass dÍslodged or washed off. Herbivorous insects, principally the larvae of a small tortricid moth (subfamily olethreutinae), ate 75-36% of deployed seeds, attacking both newly deployed seeds and hotdfast phase seedlings. Tortricid larvae grew to a-bout 4 mm Ín length. They ate the contents of the seed, hypocotyl or holdfast from within and formed a small sraxy, frass-covered dome alongside the remnant she1l of the seed or seedling. A few seedlings attacked by tortricid larvae sunrived 6 mo, because the g¡nrbs ate the seed but not the hypocotyl or holdfast. However, a signÍfícantly larger proportion of predated seeds died than unpredated seeds (Table 7.7). À few seedlings failed to establish because the hypocotyl gTres¡ asray from rather than towards the host stem (Plate 6). The hypocotyls of seedlings deployed on thin stems srere more likely to grow away from the stem than those growing on thicker stems (Fig. 7.8b). Mortality due to misdirected hypocotyl growth was more evident in wÍnter than summer (Table 7.6). Page 231 7 .3.4 Discussion Fruit structure, germination, hypocotyl growth and holdfast formation in À¡nygma quandgnq are similar to other loranthaceous and viscaceous mistletoes (Thoday 1951; Kuijt 79691 llay t977; Lamont 1983; Salle 1983). ÀIthotrgh the precise details of structure and the rate of development vary between species, the functional aspects of fruit structure, germination and seedling establishment are very similar among bird dispersed mistletoes in both families. The slow rate of development of Àmvema quandanq seedlings contrasts with the speed with which tropical mistletoes ç[roçr, but is simÍIar to several northern temperate species of viscaceous mistletoe (Docters van Leeuwen t954; Kuijt 7969). The long dr.ration of the holdfast phase coincided r.¡ith the initiat development of the endophytic system, and was accompanied by swelling of the host stem. The slow rate of growth of the western myall (section 2.6) may be partly responsible for the long developmental time in À- q¿g¡dag seedlings. Canopy growth of western myalls is highly seasonal, occuming in summer (MaconochÍe & Lange t97O), so it is likely that girth increment is also seasonal. Seasonal growbh of the host stem affects the rate of development of the primary and secondary haustoria in Viscum album (Salle 1983). Thus the rate of seedling development in Àmvemq quandanq may depend upon the season in which the seeds are dispersed. Newly established seedlings may be able to develop a more extensive primary haustorium in the host xylem if dispersed during the summer grrowing season rather than at other times of the year. The long delay in the production of aerial shoots may mean that À- qggndanq seedlings are holoparasitic upon the host during the holdfast phase. The primary haustorium of the mistletoe seedling penetrates the host bark and cortex by a combination of mechanical force and enzymatic digestion of the host tissues (Thoday 1951 ). Commonsense dictates that there must be some threshold thíckness of bark above whích seedling mistletoes cannot Page 232 penetrate. The bark on Iarge western myall stems was thicker than on thin stems (pers. obs. ) and the increasing degrree of cracking and fissuring of the bark on larger stems was probably related to the increasing thickness of the bark. The failure of ÀmyeEa quandanq seedlings to establish on branches more than 16 mm in diameter or on moderate or rough fissured stems reflected t3./ their inability to penetrate thick bark.'The increasing proportion of seedlings which died in the holdfast phase on larger stems $ras a result of the increasÍng number which lacked the resources to penetrate thick bark and died in the process. Because of the bias I showed towards smooth grey stems when deploying seeds between December 1982 and Ar.rgust 1983, a random sample of myall stems between 6-16 mm in diameter would reveal a grreater proportion of fissured stems than among those which I sampled. The proportion of stems between 6-16 mm diameter which were infected by mistletoe seeds was therefore exaggerated in relation to the establishment of seedlings on thinner stems which rarely or never exhibited fissuring. Mistletoes exhibit a high rate of esta-blishment once the seeds lodge on suitable stems for infection (Lamont 1983). Establishment percentages reported in the literature vary from 57. for Àrcguthobium tsuqense seedlings (Carpenter et al. 197Ð Lo 69?. for Viscum album in an apple orchard (Showler 197Ð. Establishment of À- quandang seeds averaged 3tz. in a period r.rhich included a severe drought. A variety of factors contribute to postdispersal seedlir¡g mortality in mistletoes, inctuding fungal decay (Lamont 1983), herbívorous moth larvae (Carpenter et aI. 7979), branch death, seed dislodgement, and developmental problems inch.¡ding germination failure, misdirected hypocotyl gnowth and seedlirg mortality in the holdfast phase (Liddy 1983). lfith the possible exception of fungal pathogens, aII of the factors above contributed to postdispersal seedling mortality in À,- çUanqaDgl. One in seven seeds which failed to establish was dislodged by unknor¡n biotic or abiotíc agents. 0f Page 233 the remainder, one-third was predated by herbivorous insects, particularly moth ]arvae, and two-thirds appeared to die as a result of developmental problems betç¡een germination and establishment. À small proportion of deployed seeds $ras parasitised by a Iarva of the predispersal seed predator, Cerapitella loranthi. Presumably the seeds had only been oviposited in recently when deployed, because fruits and seeds which were overtly parasitised by a fruít fly maggot were not deployed. The seeds of many mistletoes germinate in dry air (Kuijl 7969; Lamont 1983), as do those of À¡yema E¡g¡{anq. Considering the absence of the testa, Kuijt (1969) speculated that desiccation may be the greatest hazard faced by mistletoe seedlings during the free-Iiving phase in arid environments. The signifícant difference in establishment of seedlings between September 1982-Febn¡ary 1983 and March-Àugust 1983 r.ras proba.bly related to 2 factors: (1) exposure to high summer temperatures, and (2) the effect of the drought on parent mistletoes and potential hosts. Seeds deployed between September ard February $rere exposed to high temperatures (Fig. 2.4) either at the time of deployment or during the subsequent free-living phase, Conditions erere cooler during the germination and hypocotyl groç¡th phases of seeds deployed between late l'farch and early Àugrust. The high evaporative water loss associated with summer temperatures possibly killed a proportion of the seedlings príor to their establishing contact with the host transpiration stream. The deployment dates prior to March 1983 coincided with the drought, when parent mistletoes were probably subject to varying degrrees of water stress. The water status and nutrition of seeds produced by water-stressed plants would probably have been deficient compared to fruits produced after the drought, diminishing the chances of germination and seedling establishment. The water status of hosts also may have been deficient to the extent that some newly established seedlings could not obtain sufficient water or nutrients to survive, Ieading to seedling mortality in the holdfast phase. Page 234 Failure of the hypocotyl to orientate towards the host stem, despite vigorous grrowth, sras ê minor mortality factor in Amvemg quandanq. The orientation of hypocotyl growth in stem-parasitic mÍstletoes is generally determined by a negative phototropism in strong light, although the hypocotyl of ð- preissii is positively phototropic in weak light (Lamont 1983). Hypocotyl orientation in À- qualdanq seedlings was probably negatively phototropic since hypocotyls tended to grow away from light and toward the shade offered by the stem. Misdirected hypocotyl groç¡th was most frequent on thin stems which offered the least interception of solar radiation, and in winter ç¡hen solar radiation ç¿as least intense. The increased frequency of misdirected hypocotyl growth on thin stems r¿as partly responsible for the lower establishment percentage of seedlings on stems 1-2 mm in diameter, as opposed to slightly larger stems. Other contributing factors were the tendency for greater branch death anong the thinnest stems and a high rate of seed dislodgement, presumably due to the greater movement of such stems in the wind. The bagging of fruiting branches of ÀmveBa quandanq throughout the fruiting season (section 7.1) permitted many fruit to over-ripen inside bags and eventually to be abscised. Although seeds germinated in over-ripe fruits, the epicarp never ruptured spontaneously to release the seed either prior to or after abscission. Thus if fruits were knocked from plants or were abscised and lodged lower in the host canopy, the seedlings therein would be unable to establish. Consequently, f quandanq required a biotic agent to excise the seeds and disperse them to host branches suita.ble for infection. There are no arboreal or scansorial animals inhabiting the western myall woodlands of north-eastern Eyre Peninusla which could disperse the seeds of À- quandang other than birds. Both the spiny-cheeked honeyeater and mistletoebird consumed large amounts of fruit in the study area and were potential seed dispersers (Chapter 5). To be effective seed vectors, the species would have to disperse seeds to living western myall stems between Page 235 1-16 mm in diameter, and especially within the range, 3-6 mm. 7.4 SEED DISPERSAL BY THE SPINY-CHEEKED HONEYEÀTER ÀND MISTLETOEBIRD 7.4,1 Introduction Opinions vary as to the importance of the "quality" of seed dispersal of different frugivores in influencing the evolution of fruiting displays in plants. McKey (975) considered that differences in dispersal quality were fundamental to the understanding of different patterns of coevolution between plants and dispersal agents. tlheelwright & Orians (1982) argued that such differences as occur were generally unimportant in the evolution of the fruiting displays of plants, and were overshadowed by the potential advantages of having a broad assemblage of dispersers. Àttempts to quantify the seed shadows of different vectors have not proceeded very far (t{heelwright u Orians 1982). Two factors probably account for this. Monitoring the dynamics of the seed rain ís a difficult field of research because of the problems involved in sampling often tiny cryptic propagules in the soil seed bank (Harper 7977). Second, determining a suitable criterion by which to judge seed dÍspersal quality Ís often frustrated by the difficulty in identifying safe sites for seeds (t'lheelwright & Orians 798Ð. A suitable site for establishment may be determíned by microenvironmental variations which are difficult to detect, or by events which only take place long after seed dispersal. Despite the difficulties in quantifying the guaLity of seed dispersal, lfheelwright u Orians 1982) recognised that there were two different components to seed dispersal quality. However, they did not formally distinguish them. I term these components, seed vector efficiency and effectiveness. The efficiency of a seed vector is the probability that a seed dispersed by it will establish and grow into a mature adult. Seed vector effectiveness is the proportion of mature plants in a population Page 236 which the vector population is responsible for dispersing. Both of these attributes may be important in the evolution of fruiting displays in plants. In order to compare the role of the spiny-cheeked honeyeater and mistl.etoebird in the seed dispersal of Àmvgma ggandanq, I measured the seed vector efficiency and effectiveness of both species. 7 .4.2 Methods 7,4.2.1 Seed vector efficiency To measure seed vector efficiency, I noted the behaviour of birds which defaecated À* ggandanq seeds and recorded the following details: bird species, the number of seeds defaecated, the sites at which seeds lodged, the orientation of the seeds in space, and the distance of the defaecation site to the nearest plant of Amyema qugndanq. If seeds lodged on branches, I recorded the species of plant, whether the branch was alive or dead, stem diameter, surface texture, the angle of the branch in relation to horizontal, and the distance between the distal end of each seed and the branch. I began recording these variables at different stages of the study, so the sample sizes in each category vary. Faecal samples were obtained from spiny-cheeked honeyeaters and mistletoebirds caught in mistnets, as described in section 5,2.7. 7.4.2.2 Seed vector effectiveness Scrutiny of western myall canopies during the mistletoe population census in November 1981 (section 3.7.2) frequently revealed clumps of seeds, seed strings and individual seeds of AByema suandanq in a range of sités. Differences between spiny-cheeked honeyeaters and mistletoebirds in diet and defaecation behaviour led to species-specific differences in the stools which Lodged in western myall canopies (section 7.4.3.t), I therefore tested the possibility of using the differences to score the number of young seedlings in western myall canopies ç¡hich were attributable to each bird species. Due to time limitations, only a pilot study was attempted. Page 237 I searched three myall canopies for several hours in June 1983, and recorded the position of aII recently dispersed ÀmvCmg suandanq seedlings. The trees were censused for mistletoes in November 1981, so unlabelled foLiose seedlings were less than about 3 yr old. I measured the stem diameter of branches on which seedlings had Lodged and judged their age by reference to seedlings which I had deployed along the traverse at varying times in the previous 7 mo. I carefully examined seed remains associated with seedlings and the material adhering to fresh seedlings, noted seed orientations, and searched for zigzag viscin threads associated with seed strings which indicated deposition by mistletoebirds (see below). 7 .4 .3 Results 7.4,3.1 Seed vector efficiency Mistletoebird Histletoebirds voided Àmvema quandang seeds in a characteristic manner. Defaecating birds held their abdomen away from the perch and passed the seeds in a string which remained suspended from the cloaca. In a rapíd series of jerky motions, the cloaca was pressed against the branch several times while the bird moved up the perch. The seed string stuck to the branch at the first thrust, and the trailing viscin thread was stuck at points up the perch in a zigzag pattern. The number of abdominal thrusts varied from 1-9 and, in consequence, the length of the viscin thread up the branch varied from 1-9 cm. The only variation in this behaviour was a juvenile bird which had difficulty in ridding itself of the viscin thread after defaecating a seed. The bird eventually freed itself of the thread by repeated abdominal. thrusts, but only after dragging the thread and trailing seed 40 cm along the branch. l,fistletoebirds ate Amvema quandanq seeds throughout the year, and the number of seeds per stool varied little between months (Table 5.13). Seeds were passed in strings of. !-9 seeds, but strings of more than four Page 238 seeds were rare (Fig. 7.9), A small quantity of urates was sometimes excreted ç¡ith seeds, but other macroscopic solids çrere rarely defaecated (section 5.3.3.2). The seeds in strings adhered to each other more or less end to end, and r.rere usually defaecated and deposited on branches with the distal (hypocotyl) end poÍnting down (Fig. 7.10a). Àbout 15% of seeds slipped from seed strings while the viscin Í^ras moist and fell to lower substrates (Table 7.Ð, The orientation of fallen seeds Í¡as more even than those of seeds remaining in strings (Fig. 7.10b). In strings which stuck to branches, the top seed, i.e- the last defaecated, invariably remained stuck to the perch, so that the hlpocotyl had less than 5 mm to grrow to contact the branch. Seeds further down the string were often not touching the branch but were suspended from the seed above or by viscin threads which developed between seeds while the mesocarp sras still moist. The distance between the branch and the embryonic hypocotyl of seeds increased with the position of the seed down the string (Table 7.9), Defaecating birds tended to use near-horizontal branches (Fig. 7.tt) which were straight and unbranched, permittíng the unimpeded deposition of the viscin thread up the perch. Perch size varied between 3-22 mm in diameter but most were 5-11 mm (Fig. 7.tZ). Branches in western myaJ.l and Àmyema ryandanq canopÍes were used 63% and 27"2. of. the time, respectively (Tab]e 7.8). However, only 702" of. defaecations $,ere on live myall stems, compared Lo t6% on living À- zuandeng stems. Àbout 80% of the seeds defaecated by mistletoebirds stere dispersed to sites in the canopies of trees, shrubs and mistletoes which were unsuitable for infection (Table 7.8). About 7% vtere dispersed to live western myalt stems, of which three-quarters lodged on stems less than 17 mn in diameter (Fig, 7.73a). None of the 23 seeds (5%) which were monitored subsequently established (Table 7.t0). In most cases, the branch appeared too thick and the bark too fissured to permit seedling infection. Page 239 Spiny-cheeked honeyeater -a Like mistl.etoebirds, spiny-cheeked honeyeaters onì.y defaecated r¡hen perched. Birds passed Àmyema quandanq seeds with varying speed and ease, depending on the number of seeds defaecated. One to three seeds were usually ejected quickly in a smalt pellet with some force. Larger numbers of seeds took up to 2 min for birds to defaecate and dispose of. Spiny-cheeks perched motionless with legs apart and tail slightly elevated as the seeds were extruded. Sometimes, some or aII of the seed string feII away from the bird's cloaca, due to the mass of the seeds. At other times, the bird reached below and nipped the seed string with its biII, Ietting the seeds fa11 or smearing the string on the perch or adjacent branches. Rarely, the seeds were flicked aüray. The bird usually pecked and preened its vent prior to flying off. The spiny-cheeked honeyeater consumed Amvema ggandang seeds Ín summer mainly, and often defaecated large numbers of seeds (Table 7.77). Sixty percent of stools containing L quandanq seeds contained more than four seeds (Fig. 7.7Ð. Àbout one-third of stools consisted of the seeds only, or of seeds and urates. The rest contained the remains of fruit and seeds of other plants, insects or Lygium australg leaves in addition to À- quandanq seeds. Three-quarters of the f ouandanq seeds fell or were flicked ae¡ay. The remainder were smeared on the perch or adjacent branches (Table 7,7Ð. Consequently, the orientation of seeds dispersed to substrates in tree and tall shrub canopies were more evenly distributed (FÍq. 7.tÛc) than the seeds deposited by mistletoebirds. In this respect, seeds dispersed by spiny-cheeked honeyeaters resembled the sma1I percentage which slipped from seed strings deposited by mistletoebirds and lodged Iower in the canopy (Fis. 7.10b). Àbout 60% of. the seeds dispersed by spiny-cheeked honeyeaters lodged in tree, shrub or mistletoe canopies (Table 7.7Ð. The remairder feII into bush canopies or on to the ground. Àbout 77"¿ of. seeds were dispersed to live Page 240 western myall branches but only t.4% (6 seeds) Iodged on stems less than 17 mm in diameter. Two seedlings established on 3 and 4 mm stems as a result (Table 7.73). In both cases, birds defaecated seeds from a perch above a western myal} canopy, the seed string lodging on the phyllodes and thin branches below. Comparison of the seed shadows of the mistletoebird and spiny-cheeked honeyeater Due to differences in defaecation behaviour, the seed shadows generated by spiny-cheeked honeyeaters and mistletoebirds differed markedly with respect to the stem sizes on which seeds lodged (Fig. 7.73). Nevertheless, the proportion of seeds which were dispersed to thin western myall stems most susceptible to infection was similar for both species (Table 7,1Ð. Histletoebirds dispersed more seeds to live myall stems of intermediate infection susceptibility, because of their habit of depositing seeds on perches between 5-11 mm diameter. In addition to the two seedlings which established as a result of spiny-cheeked honeyeater dispersal, about 307. of the seeds defaecated by the species and 85% of the seeds defaecated by mistletoebirds established after deployment on suitable western myall stems (Table 7.75). The difference $ras not significant because only a small sample of seeds defaecated by mÍstletoebirds was deployed. Mistletoebirds dispersed seeds to sites in or close to esta-blished Àmyema qugndang plants more oflen than spiny-cheeked honeyeaters. Histletoebirds defaecated in |- ouandanq canopies on 18% of occasions compared Lo 6% for honeyeaters (Table 7.16>. Considering defaecations beyond f,, gge¡danq canopies only, mistletoebirds defaecated within 1 m of mistletoes significantly more often than spiny-cheeked honeyeaters. 7,4.3.2 Seed vector effectiveness Ninety new seedlings were found on the limbs, branches and phyllodes Page 24I of the three myalls, and about half were attributed to dispersal by each bird species (Table 7.77 ). Seedlings could usually be classified as mistletoebÍrd-dispersed r¡ith certainty because the zigzag viscin thread was visible alongside the seed remains. Only half of the seedlings attributed to spiny-cheeked honeyeaters were classified on the basis of exoskeleton fragments or other species of seed adhering to the Amvema qugndanq seedlings or seed remains. The remainder were classified on the basis of the number of seeds in clumps, or the position and orientation of seeds. Most seedlings judged to be less than 2 mo old were dispersed by mistletoebirds whereas most seedlings more than 2 mo old, Íncluding established seedlings more than 6 mo old, were dispersed by spiny-cheeked honeyeaters (Table 7.t7>. The branch diameters to which seedlings were dispersed tended to reflect the patterns established by observation of the dispersal of defaecated seeds (cf. Figs 7.13 & 7.75). However, the small total sample of seedlings and the tendency for seedlings dispersed by spiny-cheeked honeyeaters to be clumped were reflected in the erratic distributions. Both the mistletoebird and spiny-cheeked honeyeater dispersed seedlings which had established in myall canopies. lJith the exception of the 1-2 mo period prior to the survey, spiny-cheeked honeyeaters had dispersed more seedlings which established or $rere in suitabLe sites for infection than mistletoebirds. Honeyeaters were therefore the more effectÍve seed vector. 7.4.4 Discussion 7.4.4.1 Seed vector efficiency The mistletoebird's habit of depositing defaecated mistletoe seeds on the perch has been reported several times (North 79071 Morgan 1974; Fuller 1942>. Liddy (1983) watched birds defaecating Ànyema qua¡danq seeds in New South llales in the same manner as at Middleback. AIi (1931) and Docters van Leeuwen (1954) reported similar behaviour in oriental Page 242 flowerpeckers. Such elaborate behaviour is evidently necessary for the birds to rid themselves of the sticky seeds (Liddy 1983; Reid 1985). The behaviour of the spiny-cheeked honeyeater in defaecating !- quandanq seeds was quite different, but also indicated problems in disposal of the defaecated seeds. Large seed strings took a remarkably long time for birds to pass, and probably placed defaecating birds at considerable risk of predation. I inadvertantly distwbed a defaecating bird on one occasion. It fluttered between tree canopies with legs dangling and a large seed string hanging from its vent. The behaviour of both species pointed to the disadvantages of eating sticky mistletoe seeds. Deposition of mistletoe seeds on the perch is not an invariant trait of the mistletoebird, because its defaecaction behaviour varies wÍth the type of egesta. The small succulent seeds of Àmyema cambaqei are ejaculated by defaecating birds (Liddy 1983). Less viscid peppertree berries are often defaecated by perched birds in the normal avian manner, no attempt being made to deposit the seeds on the perch (pers. obs. ). The seed shadows of the spiny-cheeked honeyeater and mistletoebird illustrate the complexities in attempting to unravel the contributions of different animals to the seed dispersal of a plant. The general pattern of the seed shadows of the two species was quite different. Mistletoebirds dispersed most seeds to branches of a size suitable for infection, whereas most seeds defaecated by honeyeaters fell to the grround, into bushes or on to large branches. However, the reality was that most of the branches which mistletoebirds defaecated on were either dead, the wrong species or too fissured to permit seedling establishment. Seed dispersal to the stems most susceptÍble to infection stas a rare event, and the two species were similarly efficient in accomplishing it. Because of the rarity of correct dispersal, the collectíon of enough observations to accurately compare the seed vector efficiency of the two specÍes would require considerably more time and effort. Page 243 The seed shador.¡ of the mistletoebird may well be more important to other mistletoes. Most Lysiana exocarpi seeds defaecated by mistletoebirds were deposited on and adhered to the perch. The seed of L- exocami was larger than Àmyemg quandanq, producing a longer hypocotyl and larger holdfast. If seed size is correlated with a seedling's ability to penetrate thicker bark, the mistletoebird may be a more efficient seed vector of f, exogefp! at Middleback, because 75% of. defaecations çtere on live À- quandanq stems. À- quandanq is a host of L gIgcargl. 7.4.4.2 Seed vector effectiveness Seed vector effectiveness is a function of four variables: (1) the density of the population of a particular seed vector; (2) the mean number of seeds which individuals disperse; (3) the efficiency with which seeds are dispersed to suÍtable sites for eståblishment; and (4) a weighting factor which takes into account the likelihood that a seed defaecated by the vector wiII establish. Neither the spiny-cheeked honeyeater nor mistletoebird was clearly the more effective seed vector of Àmvemg quandang when all variables L,ere considered together. Seeds defaecated by mistletoebirds had higher survival rates and grrew faster, mistletoebirds dispersed seeds between autumn and spring when establishment percentages were high, and their efficiency in dispersing seeds to the full range of stems infected by seedlings ç¡as four times that of the spiny-cheeked honeyeater. However, honeyeaters were more abundant than mistletoebirds, and individuals consumed more seeds per day in summer, at least in some months. Seasonal estimates of the four variables, above, stere obtained for each species during the study. However, the associated errors were not always ascertainable, given the methods used. Calculations of seed vector effectiveness based on such estimates would have had unknown (and possibly large) errors, and were therefore not attempted. Instead, I tested the direct method of searchir¡g myall canopies for recently dispersed seedlings Page 244 to determine seed vector effectiveness. The comparative dearth of seedlings dispersed by spiny-cheeked honeyeaters in the 2 mo prior to the survey reflected the species' dietary shift to Amyema E¡andang nectar when flowering began in late autumn 1983 (Fiq. 2,2). The population density and seed consumption of mistletoebirds showed more seasonal consistency than the spiny-cheeked honeyeater, so the attenuation in the number of seedlings of increasing age dispersed by mistletoebirds presumably reflected natural attrition in the seedling population. The survey suggested that both the spiny-cheeked honeyeater and mistletoebird were important seed vectors of Xmveme sugldanq, challenging the long-held view that the mistletoebird is the principal, if not only, seed vector of Àustralian mistletoes. Indeed, the spiny-cheeked honeyeater may be the more effective seed vector in this system, as judged by a higher seed vector effectiveness in the pilot study. The honeyeater also tended to disperse seeds further from established plants than the mistletoebird. However, whether this is advantageous for Àmyeme suandanq or for mistletoes in general is uncertain. Consideration of the mechanism by which spiny-cheeked honeyeaters dispersed Àmyemq quendsng seeds suggests that the species may have been a more efficient dispersal agent prior to the introduction of rabbits and stock. Western myalI groves formerly consisted of uneven-aged individuals in aII growth stages, with the youngest individuals distributed around the edge of the canopies of larger trees. Seeds defaecated by spiny-cheeked honeyeaters in older trees and dead trees in such groves probably frequently fell and lodged in younger plants. Honeyeaters would also have been more Iikely to forage and rest in the shrub-form growth stages of western myall than mistletoebirds, because the species spends more time in structurally similar shrubs such as Exogarpos aphyllus in the present-day woodland. Hence, spiny-cheeked honeyeaters probably differentially dispersed seeds to Page 245 young hosts. The resulting mistletoes probably had the capacity to persist with their hosts for much of the life of the tree. The method of searching tree canopies for recently dispersed mistletoe seedlings proved satisfactory for measuring seed vector effectiveness, and warrants implementation in an expanded study. Most seedlings were classified with complete subjective confidence. However, objective rigour could be introduced using statistical discriminant analyses (Nie et aI. 1975) for the identification of seedlings as either dispersed by the mistletoebird or spiny-cheeked honeyeater, or of uncertain classification. The approach could be expanded to compare the tendency of each species to disperse seeds contagiously, as indicated by the spatial pattern of new seedlings in relation to established plants. Long-term monitoring of seedlings so identified r¡ould provide a unique description of the influence of different seed vectors on the structure and dynamics of a plant population. This ability to monitor the fate of Agyema SJenda¡g seeds dispersed naturally by birds, and to identify the disperser responsible, suggests that an "almost hopeless" (l,lheelwright & Orians t982) task in plant population biology might indeed be soluble. Page 246 Table 7.1 Fruit production and seed predation in the 1982 fn¡iting season. Fmit were counted on the control branches of nine plants. 4Nov 6Jan 4Mar1 7 Ar.¡g 9 Nov 16 Dec 15 Feb 81 82 82 82 82 82 83 Total no. of 198.9 177 .4 70.4 75 .7 2.7 7 .7 0 .2 fn¡it' Ripe fruilb (%> 99 .5 27.8 17.6 8.3 10.0 0 0 Fruit damaged by 5 .8 .4 1.3 7t.t 0.0 0 0 seed predators (%) " llean of 9 plants; total no. of fruit is the sum of the no. of developing and ripe fruit. o Ripe fruit includes fresh epicarp bases. Table 7.2 The proporbions of sucked (S) ard unsucked (U) seeds of Àmvema quardanq which gerrninated in different months, ar¡ tne'hypocotyl lengths after varying periods of growtñ. seeds were obtained from t4 marked plants. Nov 81 Jan 81 Mar 82 l{ay 82 Àug 82 Oct 82 Totals' SU SU SU S U S U SU SU tlean period of 37.8 L4.7 26.8 39.7 32.5 28.6 seedling gronth Dead or moritn¡rd 212s98973211270671221076 htæocotyls (t) No. of hlryocotyls dead or moriburd 53 45 34 773201 74 10 77 healthy 799 1t 28 27 23 27 13 15 8 14 91 92 NS 1.05 NS 12(1 d.f.)È .02 NS .28 NS .75 NS .02 NS .02 H¡ryocotyl ler¡gtj¡ (mn) Ìlean 6.5 6.7 2.7 2.2 8.6 6.2 5.6 5.7 10.6 7.2 7.7 7.2 95t Confiderre 5.4- 4.7- 7 .7- 1.7- 7.9- 5.0- 4.5- 4.9- I 7- 5.9- 5.1- 5.9- Inten¡aI 7.6 8.7 2.6 2.8 9.3 7.4 6.6 6.5 12 6 8.6 to.2 8.4 n 24 t2 46 35 29 34 26 29 13 76 918 F Test statistÍc' E F !' E E (d.f.) NS .085 NS 3.06** .035 NS 9.96x* 218 NS .031 (1,15) (1,34) (t ,79) (1,53) (7,27> 'Excluding Jantnry data r The tested the nul] hypothesis that the freguency of healthy seedlings was irdeperdent of 'o [2 stãtistic o sucking. rO . one-way analyses of variance (F ratios) were used to test the difference between the mean hypocotyl o were not violated. othen¡ise the t\) lengths of sr.¡cked and unsucked groups ior dates when the assumptions of anova À witóo*on two-sample test (t,) was used (Sokal ard Rohlf 1981). \¡ Page 248 Table 7.3 ComparÍson of the proportions of seeds which germinated and were healthy after 16 d of growth in the shadehouse and barn. The X2 statistic was used to test the nuII hypotheses that the frequency of healthy seedlings was independent of (1) substrate inside the barn, and (2) the location of seedlings (barn ys shadehouse). Barn Shadehouse Stick Petri Stick Petri Dead or moribund 60 77 100 100 hypocotyls (%) No. of hypocotyls dead or moribund 15 20 26 26 healthy 10 6 0 0 r (1 d.f.) (1 ) 1.00 NS (2) 17.00**x Table 7.4 The proportions of seeds defaecated by mistletoebirds (Mb) ard spiny-cheeked honeyeaters (Sc) which germinated ard survived, ard the hypocotyl lenqths of seedlings after varying periods of growth. The X2 statistic tested the null hypothesis that the freguency of healthy seedlings was independent of bird species. The F ratio tested the differences between the mean hypocotyl lengths of seedlings defaecated by the two species. Early Late Nov 81 Jan 81 Jan 82 l{ar 82 Àpr 82 Hay 82 Jun 82 Jul 82 sep 82 Oct 82 Ìrb Sc l{b Sc Hb Sc I'fb Sc l,fb Hb Hb t{b Hb Sc Hb l{ean period of 9.8 10.3 74.2 17.1 10.1 11.4 31.6 32.8 2A,5 29.7 42.7 32.4 n.r. n.r. 25.6 seedling grosth (d) Dead or moriburd 4 33 100 100 29 38 10 1s 0 6 74 77 77779 hypocotyls (u) No. of hlæocotyls dead or morih¡rd 1 28 72 33 417 3 5 0 2 39 32 5 healthy 24 58 0 0 10 18 28 28 16 31 18 43 39 16 22 x, (1 d.f . ) 6.77xx .07 NS .08 NS ONS Hræocotyl length (mn) Ìlean 5.9 4.5 4.8 3.4 7.3 6.4 7.8 7.2 6.s 7.2 9.2 8.2 6.3 95t Confiderrce 5.1- 4.0- 3.0- 2.5- 6.3- 5.2- 6.9- 6.2- 4.8- 6.7- 8 4- 7 0- 5.0- Inten¡al 6.6 5.0 6.5 4.4 8.3 7 .5 8.8 8.3 8.1 8.3 10 0 9 4 7.5 n 25 86 14 29 31 33 t6 33 77 52 42 18 27 E ratio 6.91rr 2.22 NS 1.57 NS 2.02 NS (d.f . ) (1,109) 0,47) (7,62) (1,58) Gro¡rth irdex' 0.60 0. {8 0.23 0.32 O.24 0.15 O.22 n.r. 0.2s -Ú þ la o . growth mean by the mean period of seedling growth, for N) the hypocotyl irdex was calculated as h¡rpocotyl length divided À mi st I etoebirddi spersed seedl ings. \.o Page 250 Table 7.5 Establishment percentages and stem characteristics of Ànyemg ousndang seeds deployed on western myall branches between February 1981 and Àttgust 1983, Stem characteristics: yellow-brown. y'. grey, g; smooth, sm; sli.ghtly fissured, sf; moderately fissured, mf; very fissured, vf. Stem No. of Establish- Stem characteristics diameter seeds ment' (%) (mm) deployed (ot") y/sm g/sm glsf. g/nf. g/vf. 0.5-2.4 75 28.0 60 40 2.5-4.4 184 33. 2 18 78 4 4.5-6. 4 204 32.4 3 9t 6 6.5-8.4 t47 24.5 87 t2 2 8.5-10.4 75 14.7 7t 20 I 2 79.5-12.4 43 9. 3 51 30 t9 72.5-74.4 20 5. 0 t7 77 48 t7 14.5-76.4 20 5. 0 18 6 47 35 16.5-38. 4 40 0. 0 3 3 3 92 Establishment (%) 24.3 31 .6 13. 6 0 0 'Seedlings persisted for 6-18 mo. Page 25t Table 7.6 Establishment percentages and mortality factors associated with the deployment of Amvems qusndang seeds on ç¡estern myall stems. Mortality figures are the percentages of the total number of seeds deployed on each date. Date of seed deployment 7-to 8-9 9-10 28-37 5-6 9-10 21 Jul- Sep82 Dec82 Feb83 Mar83 May83 Jun83' 4 Àug 83' No. of host branches 10 42 35 84 72 45 82 on which seeds deployed Total no. of seeds 26t 48 39 727 92 56 204 deployed No. of seedlings 35 4 363462594 established Establishment (2") 13 I 850504546 UqrleIÉv Seed predation by: Torbricid larvae 22 15 36 20 72 7 26 0ther Lepidoptera 0 0 2 4 2 7 Cerapitella loraElhi 3 0 0 0 5 0 0 Seed did not germinate I 25 23 4 5 4 4 Hypocotyl grrew weakly; 6 10 13 2 t 2 2 no holdfast formed Ì'f isdirected hypocotyl 2 0 3 2 5 9 4 growth Seedling infected 00 0 0 0 2 0 Ítself Seedling died in 3033109 I 13 5 holdfast phase Host branch died 6 001 7 0 t Seed disappeared; 10 I 81081810 fate uncertain . 95% of these seedlings were checked after 4.0-5.5 mo rather than 6 mo to determine establishment rates. Mortality fígures in these columns are conservative estimates and the establishment percentages are upper estimates. Page 252 TahLe 7.7 Comparison of the esta-blishment success of seedlings predated by tortricid moth larvae (Olethreutinae) and unparasitised seedlÍngs. The F statistic (with Yates correction) tested the null hypothesis that establishment was independent of larval predation. Seeds parasitised by tortricid moth larvee Yes No Seedlings Yes t7 777 established No 60 771 X? = 24.96***, 1 4-f^ Tab1e 7.8 The percentage of seeds defaecated by mistletoebirds (n = 447) whích lodged in various sites. DeviatÍons between the sum of the values in columns and rows are due to rounding errors. Percentage of seeds Site Defaecated FelI to Total at site site tlestern myall live branches 7.6 0 7.6 canopy dead branches 42.7 4.0 46.8 Àmvema (ruandang ]ive branches 15. 4 4.5 79.9 canopy dead branches 4.7 0 .4 5.1 Other tree & live branches 1.1. 0 1.7 strn¡b species dead branches 12.5 0.7 13.2 Bush canopy 0 0.7 0.7 Ground 0 4.3 4.3 Uncertain 0.7 0.7 1.3 TotaI 84.8 L5 .2 100.0 'The species were Casuarina qrislatg, }fygpsglg plaþvcaroum Santalum acqlinelgq!! and Lvsiana exccarpi. Page 253 Ta-ble 7.9 Relationship between the position of seeds in mistletoebird seed strings deposited on perches, and the distance of the seeds from the branch. Position of seed No. of seeds Percentage Distance from branch to in string scored touching distal end of seed' (cm) perch I t s.n. 1st (top) 37 100 2nd 27 48 0.81 t .107 3rd 21 24 7.22 ! .767 4th 7 74 2.0 ! .39 5th 2 0 3.2s t .250 'Excluding seeds in contact with the perch. Tab1e 7.10 Characteristics of the live western myall branches on which mistletoebirds defaecated Amyeme quandang seeds. ÀIl seedlings had failed to establish when checked 6-18 mo after dispersal. Date No. of seeds Branch Branch deposited surface' diameter swvived (mm) 6-18 mo 29 Apr. 81 3 sf 7 t yes 29 Apr. 81 7 sm 5 1 yes 26 Jan. 82 3 mf t 0 0 yes 25 Mar. 82 7 n.r I 5 yes 26 Har. 82 2 mf 9 2 yes 22 Apr. 82 7 vf. 7 2 1 no 14 May 82 A sf I 0 yes 23 Jun. 82 3 mf n r yes 2t oct. 82 t vf 7 9 7 yes 10 Dec. 82 t sm 7 I n.r 5 May 83 3 sm 7 0 3 yes 'Smooth, sm; slightly fissured, sf; moderately fissured, mf; very fissured, vf; data not recorded, n.r. Page 254 Ta.ble 7.11 Number of lmyemê SJandang seeds in faecal samples from mistnetted birds and field õotGðtiõñs in the study area. Data are the mean t S.E. Sample size in parentheses. Spiny-cheeked honeyeater l{istletoebird Mistnetted Field Mistnetted Field bírds' collections b birds' collections b Jan 6.3 1 .9 (9) 10.7 ! 2.0 (12) 2.5 ! .2 (17) Feb 77.7 ! 7.6 (2) 2 (1) l{ar 4.8 t 2.6 (4> 3.9 t 1.0 (10) 2.6 ! .5 (16) Àpr 3.5 t 1.0 (10) 3.0 t .4 (9) (20) May 0.1 1 .1 (8) 0.2 ! .2 (6) 1.8 I .8 (4) 2.7 ! .3 Jun 0.6 t .3 (7) 1.9 t .4 (14) JuI 0.3 1.3 (11) 0 (4) 3.0 t 1.0 (2) 2.6 ! .5 (22) Àug 0 (1) 1,6 ! .5 (7) sep 1.0 t .7 (9> 4.2 ! 7.7 (6) 2.3 ! .9 (3) 2.8 ! .2 (41) 0ct 4.0 ! 2.7 (3) 2.8 ! .3 (16) (8) Nov 5.8 t 2.0 (i) 8.0 I 1.4 (18) 4.0 I 1.0 (3) 3.9 t .5 (10) Dec 9.7 ! 3.5 (6) 9.7 ! .9 (3) 2.2 ! .3 .Birds were mistnetted in December 1980 and bimonthly between November 1981-November 1982. b0bservations spanned JuIy 1980-Àugust 1983. Page 255 Tahle 7.72 The percentage of seeds (D = 477 ) which lodged in various sites after defaecation by spiny-cheeked honeyeaters. Deviation between the sum of the values in columns and rosrs are due to rounding errors. Site Percentage of seeds Deposited Fell to Total at site site I{estern myalI Iive branches 0.2 10.6 10.8 canopy dead branches 5.8 10.8 16 .5 phyllodes 0 2.9 2.9 suspended 7.4 0.2 7.7 Àmvemq cmandang live branches 3.6 0.7 4.3 canopy dead branches 1.0 0.5 7.4 foIÍage 0.5 0.5 1.0 suspended' 2.9 0 2.9 Other tree & Iive branchesb 0 4.t 4.7 shmb spp dead branches 7.9 5.5 13.4 foI iage 0 0.7 0.7 suspended' 0 0.2 0.2 Bush canopy 0 9.6 9.6 Ground 0 30.5 30.5 TotaI 23.3 76.7 100.0 'Seeds suspended by viscin threads ) 4 cm from a substrate. b The species were fuçgEpos ephvllug and Myqpezum platvgq¡g¡B. Table 7.13 Fate of Amvema quandanq seeds dispersed by spiny-cheeked honeyeaters to the live brarrcñeã of western myall and Exocarpos aphvllus. Seedling survival was monitored 6-18 mo after disPersal Date No. of Branch No. of Host branch seeds Host' surface b diameter seedlings survived dispersed (mm) established 29 Apr 81 2 Acpa vf 13.1 0 yes 29 Apr 81 5 Àcpa vf t 8.6 0 yes 29 Àpr 81 t Àcpa vf 2 1.6 0 yes 12 Nov 81 6 Exap n.r 7 2-2.5 0 yes 24 llar 82 3 Acpa gm 2.5 7 yes 15 Sep 82 3 Exap n.r 7.7 0 yes 16 Apr 83 7 Acpa sf 9.9 0 yes 18 Àpr 83 2 Àcpa (phyllo des) 0 (shed) 18 Apr 83 t Àcpa SM 3.6 1 yes 18 Àpr 83 9 Acpa (phyIIo des) 0 (shed) 15 Nov 83 7 Acpa mft j.6 0 yes 'Àcpa, westenl myall; Exap, EfgqeEpqg aphvllus. b Àbbreviations as in Table 7.LO. Page 256 Table 7.14 The percentages of Àmvema EJalldang seeds dispersed by mistletoebirds (n = 447 ) and spiny-cheeked honeyeaters (l = 477 ) to varying sized live branches of western myalI, 1980-1983. Stem diameter Histletoebird Spiny-cheeked (mm) honeyeater 0.5 - 2.4 0 0 2 2.5 - 4.4 0.7 t 0 4.5 - 6.4 0.2 0 6.5 - 8.4 1.8 0 8.5 -10.4 2.2 5.8 0 2 7.4 70.5 -12.4 0.9 0 72.5 -14.4 0 0 74.5 -16.4 0 0 16.5 -18.4 0 0 18.5 -20.4 7,7 2 6 ¿ 20.s 0 6 7 rrot recorded 9.7 0 Table 7.15 Estabtishment of Àmyena quandang seedlings from seeds defaecated by birds. Seeds were deployed on western myall stems 2-15 mm in díameter. Mistletoebird Spiny-cheeked honeyeater No. of stools t 76 Nov 82- no. of seeds 4 136 deployed Feb 83 No. of seedlings 4 38 established No. of stools 4 I lfar 83- No. of seeds 9 24 deployed Jun 83 No. of seedlings 7 8 esta-blished Establishment (%) 85 29 Page 257 Table 7.16 2 x 2 Contingency tables comparing the number of defaecations by spiny-cheeked honeyeaters (Sc) and mistletoebirds (l,fb) in relation to the position of Àmvema EJandalg canopies (Àq). The f;statistic tests the nuII hypotheses that (1) the frequency of defaecations within l- quandanq canopies is independent of bird species, and (2) the frequency of defaecations less than 1 m from À- gganda¡g canopies is Índependent of bird specÍes. The data in (2) only includes defaecations beyond ¡- E¡andar¡g canopÍes. Yates correction was applied in both tests. Bird species x" Sc Mb (1 d.f-) llithin Àq 6 35 Number (1 ) 6.73** Beyond Aq 90 155 of defaecations (lmfromÀq 0 72 (2) 7.22x* )lmfromAq t7 10 Table 7.1,7 The number of Àmvema quaDdanq seedlings of varying age found in western myall canopies in June 1983, and attributed to misletoebird and spiny-cheeked honeyeater dispersal. The number of seedlings classified with complete confidence êre shown in parentheses. Seedling age (mo) TotaI Bird 0-2 2-6 6+ Holdfast Foliose Dead branches 19(19) 0 0 0 l{istletoebird ÀIive branches 27(?5) 1(0) 2(1) 1(0) TotaI 46( 44) 1(0) 2(1) 1(0) 50( 45 ) Dead branches 0 15( 11 ) 0 0 Spiny-cheeked Alive branches 5(0) 4(1) 7(5) 6(0) honeyeater PhyIIodes 3(3) 0 0 0 TotaI 8(3) 79(1?) 7(5) 6(0) 40( 20 ) Page 258 'a Ep 1 Me Per mm En \ I t I I \ I I I Emb I I , \ I \ I, \ I Ss Ped Fig. 7.1, Longitudinal section of the mature fruit of Àmyerng SJeÉeDg shówing the embryo (Emb) Iargely enclosed in the endosperm (End) and the glandular hypocotyl (Hy) protruding into the mesocarp. The main parts of the pericarp (Per) are the outer rind or epicarp (Ep), the fleshy mesocarp (Me) and the endocarp (En). Cotyledon (Co); peduncle (Ped); seed stalk (Ss). Page 259 1981 Fruiting season 40 l- l o fr 6 1982 Fruiting season tr Itr ltl olJ. z :) o 3 M AMJJASO NDJF 1983 Fruit 1981 Þ 3o0 rtr- f É TL TL o 2 00 zF l o 100 MAMJJASONDJF 1982 1983 Fig. 7.2. Successive fruitÍng seasons of 9 marked plants of Ànyetne quandang. The amount of young and ripe fruit is plotted for the 1981, t982 and 1983 fruiting seasons. The periods of ripe fruit production are indÍcated by the solid black bars. In 1981 and 1983, the data are the mean number of young and rÍpe fruit per plant on control and caged branches. For 1982, the mean number of fruit per plant on control branches is plotted as a proportion of the original number of buds. Young fruits C-O-); sum of young fruit, ripe fruít and fresh epicarp bases (---). ltr lr¡ 6 o 4 àe oz fuJ ø 2 fruJ lL j uJ tÍ. o s ON DJFMAM JJ ASOND JF 1981 1982 1 983 Fig. 7.3. Rate of the reduction in the nr.¡mber of developing and ripe fruit -o on control branches of 9 marked plants in the 1982 fruiting season. The qÞ black bar indicates the period of ripe fruit production. Àrea of the o histogram bars is proportional to the reduction in the guantity of fruit. qrw O a Page 261 16 12 z fL frBfL CJ) 3 ts l fr l! 4 2 1 o S ON DJFMAM JJ ASOND 1981 1 982 Fíg. 7.4. The standing crop of ripe fruit (includes fresh epicarp bases) on coñtrol branches of 9 marked plants during the 1982 fruiting season. The ripe fruit crop is partitioned a¡nong the first 5 cohorts of fruit set during flówering in 1981 ard identified in Fig 7.6. Most branches were bagged, excluding fnrgivores and seed predators, between early January and early Harch 7982. Page 262 20 (a) 16 zt- 12 fL cÍ LrJ ÍL I oz 4 0 100 93 (b) s 80 ô I,JJ 60 o 123 20 I,JJ E 40 27 t- :) cÍ 20 ]L I 25 95 o ND JFMAM JJ ASON 1981 1 982 Fig. 7.5. (a) The number of ripe fn¡it (O) and fresh epicarp bases (a) on coñtrol branches of. 74 plants during the 1982 fruiting season. (b) The percentage of ripe fruit on newly ex osed branches removed by birds within 2l nr after b.gging. The total number of fruit exposed on 8-13 plants on each occasion is shown alorgside the respective points. .01 (a) 2 1 o 3 o 4 5 z 0 LtJ f .0 1 ø (b) [rJ É. IL j frLrJ o MAMJJASON 1981 Fig. 7.6. Frequency distributions of (a) flower turnover during the 1981 flowering season unä Cn> of the resultant amount of fruit set per day on branches òf 9 marted plants. The number of fruit in the 6 cohorts -o control (the 0 was measured in late Septembei (first cohort) or in early November a remainder). Flower turnäver and seed set were significantly correlated o N) (r < o\ = .90, ! = 6, ? .01). (¡) Prye 264 1.0 lt¡ ¡¡¡ 1 .5 I0 ¡¡t rll 2 ë4 s ', .3 uJ ttt t¡t f, 3 ø llJ ïocÉ d.4 4 fr trl II o .5 5 tll¡ rll I¡I¡I o .5 o S O N DJ F M A M J J A S o N D J F 1981 1 982 1 983 Fig. 7.7. Rate of dissipation of fruit in the 6 cohorts (see Fig. 7.6.) on coñtrol branches of 9 marked plants dr.¡rir¡g the 1982 fruiting season. Black bars indicate the periods in which ripe fruit were recorded. Page 265 1.0 o (a) o o o o o o o z ooooooooo o l'U =o 0 trl E l'L o.5 j (b) ul fr o o o o o ooo o o 2 468101214 16 18 STEM DIAMETER (mm) Fig. 7.8. Relationship between stem girth and the proportions of Àmvemg quándalg seedlings wtriËh died (a) in the holdfast phase prior to õtãSTÇhment, oi <¡l as a result of misdirected hypocotyl growth. correlation coefficients! (a) E = 0 .47, ? S .05, n =18; (b) E = -0'69' PS.001,n=18. 60 n=181 oz lTU o (ruJ lJ. 20 o o123456 789 NO. OF SEEDS / STOOL Fíg.7,9. The frequency dÍstribution of the number of Amvema (ItlardaDg seeds pei stool defaecated by mistletoebirds, 1980-1983. Page 266 4 (a) 3 n=231 2 1 0 oz [ü f o 2 (b) uJ n=29 E, l! J 1 tu É 0 2 (c) n=117 1 0 20 60 100 140 180 340 300 260 220 180 Hypocotyl up HypocotYl down SEED ORIENTATION (") (a Fig. 7.10. The orientation of seeds dispersed by mistletoebirds & b) ar¡d honeyeaters (c). Seeds deposited in strings are sho$rn in (a) an¿"pínv-ån"eked see¿s which feII to lower substrates or $rere smeared on substrates with the bÍII are shown in (b) and (c). Page 267 2 o z n:131 flrJ o uJ fr 1 tL j LrJ E. o 30 60 90 Horizontal Vertical DEGREES ABOVE/BELOW HORIZONTAL Fíg.7.17. The angle of the perches, in relation to the horizontal, used for defaecation by mistletoebirds. 2 n=146 oz l¡J f o 1 ul (E lJ. frUJ 24 6810121416182022 PERCH DIAMETER (mm) Fíg. 7.12. The size distribution of defaecation perches used by miÃtletoebirds. LÍve western myall stems (black); dead myall stems (grey); Àmvema quandanq stems (stripe); other (open). 2 Page 268 n=4O6 (a) 1 oz trJ lll'flTfrl: aoul fr lJ. j t¡J OE n=364 (b) 1 tttttm o 2 46810121416-l¡ii4ll¡IEll 18 'oìo BRANCH DIAMETER (mm) Fig. 7.13. Seed dispersal to varying sized stems by mistletoebirds (a) and spiny-cheeked honeyeaters (b). Live western myall stems (black); dead myall stems (grey); Àmvema E¡andg¡g stems (stripe); other (open). n=54 oz ruJ .1 af LrJ 1al 25 rÍ. lJ. j uJfro T 2 4 6 8 1 1 4 1 I NO. OF SEEDS/STOOL Fíg.7.14. The distribution of the nunber of lmyeme qYaF+q seeds in the stóols of spiny-cheeked honeyeaters. Stools which consisted entirely of À- SJandang reãds-and urates (black); stools which also contained arthropod exosXeteton, the fruit remains and seeds of other plants or Lvcium australe leaves (open). Page 269 (a) 1 oz fTJJ ø 0 [rJ E LL j (b) [rJ(r 1 o t I 20 2 4 6 I 10 12 14 16 18 20 BRANCH DIAMETER (MM) Fig. 7.15. Dispersal of Àmygrne qugndang seeds (n = 90), attributed to miãtletoebirds la) and splny-chee[ea noneyeaters (b). to varying sized stems of western myall. Established seedlings (closed); seedlings ( 6 mo old (open). CHÀPTER g CONCLUDiNG DISCUSSION 8.1 MUTUÀLISH BETI,IEEN ÀMYEUÀ OUANDÀNG, AND THE SPINY-CHEEKED HONEYEÀTER ÀND MISTLETOEBIRD The preceding chapters reveal an extraordinary degnee of mutualism between AmveBg quandang and two bird species. the spiny-cheeked honeyeater and mistletoebird. The birds receive a permanent carbohydrate resource in fruits or nectar, and the plant maintains permanent populations of dispersers (mistletoebird) or pollinators-cum-dispersers (spiny-cheeked honeyeater). The interaction between [mvemg quandang and each bird is facultative rather than obligate. In the study area, neither individual plants nor birds are obligately dependent on their mutualistic partners. Spiny-cheeked honeyeaters and mistletoebirds obtain most of their carbohydrate requirements from !- quandang fruit or nectar, but also feed on the fruit or nectar of minor food plants. Furthermore, although individual spiny-cheeked honeyeaters are site-specific and probably hold life-Iong territories centred on À- quandanq plants, individual mistletoebirds are less dependent on the local population of plants and more nomadic. From the plant's viewpoint, A- crusndsng is pollinated principally by the spiny-cheeked honeyeater which effects most seed set, but other honeyeaters, insects and possibly the agency of autogamy are potential sources of seed set. The seeds are dispersed by both the spiny-cheeked honeyeater and mistletoebird. Thus, if either (but not both) of the bird species were removed from western myall woodland, À- E¡anda¡g would probably persist in the community. Likewise, if A- suandang sras removed, both birds would probabty continue to occur, albeit in much reduced densities and on a seasonal basis only. The interactÍons between the three species are more clearly facultative ç¡hen viewed from a regional perspective. In the tlhyalla region, Page 27I mistletoebirds reside in mallee open-scrub in the Middleback Range during the fruiting season of À* miquglii, and some spiny-cheeked honeyeaters hold territories based on flowering Eremophilg aller¡ifofiq on rocky hills, and on E. Ionqifolia in broad watercourses, during the spring and early sunmer f lowering seasons respectively. Furthermore, the spiny-cheeked honeyeater and mistletoebird oecur across large areas of Àustralia where À- quandang is absent (cf. Barlow 1966; Blakers C! aI- 1984), and A- ruqnde¡q occurs in sclerophyll forest in temperate Victoria in the absence of the spiny-cheeked honeyeater (Bernhardt g Calder 1981a). t'lhether any Àr çluanda¡S¡ populations exist in the absence of the mistletoebird is unknoq¡n. Despite the facultative nature of the interactions, the degree of reciprocal dependence between Amyema zuendgng and its two avian associates appears to be exceptional anrong vertebrate-plant mutualisms. Recent reviews have stressed the improbability of one-to-one dependence between plants and their animal pollinators and dispersal agents on theoretical grounds, anrl the rarity of such mutualisms in the natural world (Janzen 7975,1980; I'theelwright & orians 1982; Howe 1984). The only welI documented instances concern invertebrate pollinators and their host plants (Janzen 7975; Boucher et eI- 7982; Howe 1984). The one-to-two dependence betç¡een À- zuandêng and the spiny-cheeked honeyeater and mistletoebird is as close to a monophilic mutualism involving vertebrates and higher plants as yet reported. However, further study of the reciprocal dependence betç¡een the white-cheeked cotinga and mistletoes in the Peruvian Andes may reveal an even tighter dependence between bird and individual mistletoe species in various localities (Parker 1981 ) . I'lhat are the unusual features of the interaction between Àmyeme zuendelq and its two mutualists which set it apart from most mutualisms between vertebrates and their food plants? From the point of vieç¡ of the mistletoebird, À, zugndCng provides a continuous supply of ripe fruit. Few vertebrate food plants produce f lowers or ripe fruit yeår-round (l,lheeÌwright Page 272 & Qrians 1982; Bawa 1983) with the exception of some species of early successional vegetation in the tropics, which flower continuously and are pollinated by hummingbirds (Feinsinger 1976; Opler et el- 1980; Feinsinger et af- 1982', Bawa 1983). Few frugivorous or nectarivorous vertebrates are as oligotrophic (have as restricted a diet) as specialised mistletoe-feeding frugivores. Thus the probability of an oligotrophic vertebrate finding a food plant which produces a year-round crop of fruit or flowers is small. From the point of view of the spiny-cheeked honeyeater, Àmvema suandanq provides a contÍnuous supply of either ripe fruit or nectar. Although many plant taxa in the tropics and southern hemisphere are both pollinated and dispersed by vertebrates, few animals are both effective potlinators and dispersal agents of plants. Examples are the Iarger honeyeaters (Pyke 1980; Chapters 5-7), flowerpeckers (Doctors van Leeuwen 19541 Kuijt 1969; Davidar 1983a) and whíte-eyes ZosteEops (Sargent 1928: Paton & Ford 1977; Garnett & Rooke 79821 Davidar 1983a). Larger animals such as emus (Davies 197Ð and the brushtail possum Trichosurug vulpecula (V. Turner pers. comm. ) which are attracted by both fruit and flowers tend to destroy the flowers they feed on. The reproductive attributes of Amyema quandanq underpins the interactions between it and the spÍny-cheeked honeyeater and mistletoebird. The fruiting display is characterised by the tempered, year-round production of relatively large, cryptic fruit. More ripe fruit are produced in summer than dwing the protracted winter flowering season. These features may have evolved to accommodate one or more sedentary populations of dispersal agents which have a larger requirement for fruit in summer than winter. The size of the fruits of À- quandsng evidently excludes smaller partial frugivores such as the singing honeyeater from consuming the seeds and thus functioning as seed dispersers (section 5.4.1). The mistletoebird is only a recent arrival on an evolutionary time-scale, and probably has had little effect on the evolution of the plant's fruiting display (section 1.5). The birds with Page 273 which A- quandenq most likely evolved are larger honeyeaters similar to the present day spiny-cheeked honeyeater, and specialised frugivores such as the painted honeyeater which coevolved with Australian mistletoes and specialises on a diet of mistletoe fruit (section 7.4.1). The distribution of the paÍnted honeyeater presently overlaps the range of À,. quqndenq in eastern Àustralia (cf. Barlow 7966: Blakers e! eI- 1984). The spiny-cheeked honeyeater is not the only moderately large, sedentary and partially frugivorous honeyeater within the range of A- quandaDg. The yellor¡-throated miner lanorina flaviqula resides in western myall woodlands on Middleback (Appendix 2) and on the north-western Nullarbor Plain (Brooker et ef- t979), and feeds on mistletoe fruit (Reid 1985) as ç¡ell as nectar, insects and other kinds of fruit (Pyke 1980; pers. obs.). ÀIong with the spiny-cheeked honeyeater, it probably typifies the guild of birds with which f quandanq evolved. The flowering and fruiting display of Amyema cnJendanq is the result of various selection pressures acting at different stages of the life cycle. À- quandang is the only abundant nectar producing plant for birds in the western myall woodlands on north-eastern Eyre peninsula. Occasional individuals of Eremophila opnositifolia, !, lonqifolia and patches of Lyglgna exocaEp! and A- miraculosuB occur, but these provide a negligible resource in comparison to the fn¡it and nectar produced by À- quaûlgng. This situation contrasts strongly with other pollination systems involving honeyeaters in southern Australia, where birds pollinate and are dependent on a guild of nectar producing flowers (Ford & Paton 1985). I suggest that in the absence of other plants capable of attracting a high density of pollinating honeyeaters, there is an evolutionary advantage for f $andanq to sustain a high density of larger honeyeaters year-round to double as pollinators and seed dispersers, rather than to attract large numbers of pollinators and seed dispersers from adjacent regions during distinct flowering and fruiting seasons. Surrounding habitats (rocky hills, Page 274 watercourses, chenopod steppe, sandridge desert, dongas) proba-bly could not provide the density of honeyeaters, on a seasonal basis, which is sustained permanently by L quandang in myall woodland. The advantage of sustaining a sedentary population of larger honeyeaters has probably been reinforced by the occurrence of drought. Dry conditions can alter the timing of flowering in Àmvema qugndanq by up to 4 mo in some years. If a plant such as À- quandanq was relíant on a nomadic or migrratory pollinator, the pollinator would face periods of resource shortage in years when flowering was delayed, follor.red by periods in which the plant species was probably competing with other flowering plants for the pollinator's attention. By staggering fnrit production and flowering, Amyema quandang has sedentary dispersers available dwing the main fruiting period, r¿hich become its pollinators whenever flowering begins. Drought may have enhanced the advantage of continuous fruiting in a second way. Dry conditions may occur at all times of the year and, similarly, drought-breaking rains can fall at any time. If the likelihood of seedting establishment varies with seasonal conditions, year-round fruiting may maximise the chances of some seeds being dispersed whenever conditions are best for establishment. There are two apparent anomalies in the fruiting display of Àmvema E¡andg¡g. Most seeds are dispersed in summer when conditions for seedling establishment are probably least propitious due to high temperatr.rres. The disadvantage of summer fruiting is probably a trade-off against the combined advantages of year-round fruiting, winter flowering, and advantages associated with summer fruiting. Most mistletoes Ín arÍd South Australia flower in winter (Reid 1985). Three mistletoes with surnmer flowering seasons in southern temperate habitats flower in winter in the arid north of the State. There appears to be a selective premium on winter flowering in the arid zone for three reasons. (1) Nectar would quickly evaporate urder high summer temperatures, especially in the open flowers of Àmvema. Hence the Page 275 attractant for bird visitation ç.rould be non-functional on hot days except in the early morning. Q) BÍrds are of primary importance to L cruandanq as pollinators, whereas most insects which visit its flowers are best considered pollen and nectar thieves. l,linter flowering lessens losses of nectar and pollen to inefficient pollinating insects. (3) SmaII ants Iridomyrmex sp. (gp F) may be so abundant and pugnacious on flowering Lvsiana exocarpi in late sunmer at Middleback that they repel flying insects which land on the flowers, and attack honeyeaters and interfere in their foraging bouts at flower".t*/ There are also advantages associated with sunmer fruiting. Spiny-cheeked honeyeaters drink frequently at station troughs on very hot days (section 5,3.2.6). Larger honeyeaters would be expected to exhibit a strong preference, if not a reguirement, for succulent foods in hot weather in order to maintain water balance. It is doubtless less costly to the water economy of a mistletoe to package water in succulent fruits inside an impervious rind than to provide a similar amount of water as floral nectar, much of which would be lost by evaporation and to insects. The other apparent anomaly in the fnriting display of Amvema ggandanq concerîìs the ripening of fruit across the flowering season. The spiny-cheeked honeyeater prefers nectar to fruit when both are available, suggesting that simultaneous flowering and fruÍting seasons in winter would not }ead to successful seed dispersal by honeyeaters. Nevertheless, spiny-cheeked honeyeaters consume a small guantity of seeds during the flowering season. If the chances of seedling establishment are higher in winter than summer, there would be selective pressure on plants to ripen as many fruÍts as were likely to be taken by honeyeaters dr.rring the flowering season. tlinter fruiting may also have evolved to attract a specialist frugivore tike the painted honeyeater or, alternatively, may be a recent and evolving feature in response to the year-round presence of small numbers of mistletoebirds. Page 276 Neither the spiny-cheeked honeyeater nor mistletoebird display superficial adaptations which are likely to have arisen through interactions with Àmyema quandanq or other Àustralian místletoes. However, the most distinctive adaptations of fnrgivorous birds to a diet of fn¡it generally relate to the structure ard function of the gastrointestinal tract (Zistriler & Farner 1972', Herrera 1984b; section 7.4,7). The mistletoebird arrived in Australia r¡ith a long coevolutionary history of interactions with oriental mistletoes, and was preadapted to feeding on the fn¡its of most Àustralian mistletoes, inch.rding those of L quandanq. It is unlikely to have coevolved with f,* suandanq or other Àustralian mistletoes. There have been no anatomical studies of the alimentary canal of the spiny-cheeked honeyeater. The species may exhibit gastrointestinal adaptations related to fnrgivory, considering the amount of fruit in the diet (section 1.6; Chapter 5). However, f quandanq seeds are only one of many fn¡it types, along with insects and nectar, which would have influenced the digestive anatomy of the species. Thus the spiny-cheeked honeyeater is not coevolved with À- suandanq in a monophitic sense. Due to dietary generalisation and the stabilising effects of gene-flow across the whole of its range, coevolution of the spiny-cheeked honeyeater with the Australian flora (Iike other species of larger honeyeater) has been diffuse. The reluctance of most opportunistic frugivores Ín the community to consume Àmyema ouandanq fruit in guantity is intriguing. Smaller species are probably unable to ingest or pass the seeds safely and the foraging efficiency of larger species in the dense thin-stemmed canopies may be low (section 5.4.1). The net advantages or disadvantages to À- quendanq of the exclusion of potential species of seed vector from the disperser spectnrm are uncertain. The singing honeyeater is broadly similar in diet and behaviour to the spÍny-cheeked honeyeater and would probably generate a similar mistletoe seed shadow. Further studies are reguired to determine ç¡hat factors exclude opportunistic frugÍvores such as the singing honeyeater Page 277 from consuming the fruits of À- quandanq and lvsianq exocarpi. In summary, the key features which set the interactions between funygma quandaDg, the spiny-cheeked honeyeater and mistletoebird apart from most mutualisms between vertebrates and their food plants are: (1) the abundance of À^ ggandanq in western myall woodland in relation to other nectar producing plants for birds; (2) the year-round production by À- zugndcnq of the primary source of fruit or nectar for spiny-cheeked honeyeaters and mistletoebirds; (3) the facultative specialisation of the spíny-cheeked honeyeater and mistletoebird for ç q¿andang fruit and nectar; and, (4) the reluctance or inability of other frugivorous birds in the community to consume A- quandang fruit in quantity. The third featwe r¡ould probably be common among vertebrates if more of their food plants flowered or fruited year-round, The oligotrophic diets of the spiny-cheeked honeyeater and mistletoebirrl in the study area involve no evolutionary specialisation on the part of the birds to feed specifically on À- quandanq nectar and fruit. The second feature is probably an evolutionary outcome of various selection pressures on À* ouandanq in the presence of larger honeyeaters which are both effective pollinators and dispersers. The first feature would appear to be largely a matter of chance, since there is no evidence that À^ quqndanq competitively excludes other nectar producing plants from the community. The occurrence of only one species of nectar or fruit producing plant might often be expected in ecosystems with comparatively small numbers of long-Iived species, such as island and desert conrmunities. Both t{heelwright & Orians (1982) and Howe (1984) speculated that the pairuise reciprocal evolution of specÍes pairs might generally be restricted to such situations s¡here plants and animals can coexist for a long time without interference from competitors. Page 278 'a 8.2 THE EVOLUTION OF SPECIALISED },f ISTLETOE-FEEDING FRUGIVORES The dietary specificity of the frugivorous birds which specialise on epiphytic mistLetoes in various parts of the world (section 1.4.1) is atypical among frugivores. Wheelwright & Orians (982) argued that finely tuned mutualistic relationships in seed dispersal systems should be rare for the following reasons: (1) the inability of the plant to provide 'incentives' for precision in seed dispersal', (2) the relatively smalI differences among frugivores in seed dispersal quality; (3) the unpredictability and difficulty of recogmition of suitable targets for seeds;(4) the potential advantages of having a broad assemblage of dispersers; and (5) the longevity of seed dispersing vertebrates, Ín contrast to the short life cycles of the insects which are parb of highly specific pollination systems. t{hat is different about mistletoe dispersal systems that selection should have favoured the evolution of birds which solely or primarily eat mistletoe fruit? Clearly, mistletoe dispersal systems differ from those of terrestrial plants in three major respects. (1) Safe sites for mistletoe seeds are precisely defined, !,e. the smaller Iiving branches of compatible host species. (2) The viscidity of most mistletoe seeds Ís the 'incentive' to encourage dispersers to deposit seeds on the perch, either by defaecation as in the flowerpeckers, by smearing and bil}-wiping as ín the spiny-cheeked honeyeater, or by regrurgitation as in the white-cheeked cotinga (Parker 1981) ard tinkerbirds (Godschalk 1983b). (3) The seed shadows of the frugivores which disperse mistletoe seeds may differ dramatically with respect to branch síze, as illustrated by the Àmvema quandanq seed shadows of the mistletoebÍrd and spiny-cheeked honeyeater. Presumably, selection of mistletoe reproductive traits has favoured the consumption and dÍspersal of seeds by those birds which are more likety to deposit seeds on suitable branches. Selection, in turn, would have favoured more efficient fruit handlinq ard passage of seeds in birds Paqe 279 whose diets largely comprised mistletoe seeds. Thus, mistletoes should -a benefit from higher guality dispersal by specÍalised mistletoe feeders, and the latter ought to be more efficient at handling and passing the seeds than other frugivores. There is evidence in support of both these predictions (tlalsberg 7975; Parker 1987; Godschalk 1983b). 8.3 HOSTS ÀND HÀBITÀT STABILITY ÀIthough it is generally appreciated that stem-parasitic mistletoes are not subject to some of the important selection pressures which affect the evolution of terrestrial plants (Barlow 1981 ), Iittle consideration has been given to the factors which are most influentÍal in determining mistletoe tife history strategies. Like aII parasites, a mistletoe is dependent on the survival of its host. More crítical, still, is the survival of the branch parasitised by the mistletoe. Un1ess a mistletoe or the host can influence the survival of infected branches, the demognaphy of the mistletoe populatíon must closeJ.y reflect the demogrraphy of the branches of the host population (Chapter 3). These considerations suggest that the longevity of the host population may be a critical determinant of the 'stability' of the habitat for mistletoes. Similarly important may be tree architecture and the patterns of development of branches and their abscission in the host population. For instance, a grreater proportion of the older (lower) branches of a young tree growing upwards to take a position in a forest canopy would be a-bscised than for a similar woodland tree (Àddicott 797Ð. À mistletoe parasitising a branch of a woodland tree would, on average, Iive longer than one which established on a forest sapling, other things being equal. Host and branch longevity may select for various life history traits in stem-parasitic mistletoes, including haustorial structure, modes of vegetative persistence (section 3.1.4.3), breeding system (section 6,7,4.1) and seed set ratios (section 1.3). The stability of the habitat of Page 280 mistletoes is also influenced by the natural catastrophes which affect terrestrial plants, such as bushfires and cyclones. Nevertheless, in the western myall woodlands, host longevity and the demography of the host branch population probably impose the upper limit on the potentiaJ. lifespan of individual Amyema ggandgnq. 8.4 BIOLOGICÀL PROCESSES ÀND ÀRID ENVIRONMENTS The annual reguJ.arity of reproduction in Àmyema quandang and its persistence wíth reproductive activity in a severe drought are at odds r¡ith the popular notion of opportunistic reproduction in arid zone perennials. Host of the perennials considered in Chapter 4 displayed seasonal flowering or fruiting, although drought curtailed the reproductive output of all species to a greater extent than f quandang, The results for A^ quandanq and most of the other specÍes failed to support the predictions of the arid zone unpredictability hypothesis. Enough studies of arid zone pJ.ants and animals have been completed to indicate that there are multiple ways to succeed (i.g. survive) in the arid zone (Davies 7i76b, 1982). Moreover, the phenologies of most plants are tied to regular environmental cues, and most animals depend on regrular resources available on a local scale. The general hypothesis of an unpredictable arid environment and its associated predictions need to be replaced with more specific models, preferably ones which have a mechanistic basis and admit the possibility of multiple states and therefore multiple outcomes. In the search for a more predictive science, the discussion in section 4.4.4 of the drought response of Amyema zuardgng and other perennÍals suggests a possible framework in which to explore the reproductive patterns of arid zone plants. There, I argued that the pre- and post-drought responses of the species srere largely explicable in terms of three attributes: (1) the timing of significant rainfall in relation to the reproductive cycle; (2) the seasonal period in Page 281 which bud initiation could occur; and (3) the time between successÍve stages of the reproductive cycle from bud initiation to ripe fruit production. tfith additional information relating (a) rainfall to soil moisture (Noble 7979), and (b) soil moisture to reproductive performance, it would be possible to use knowledge of a plant's phenological attrÍbutes to predÍct its reproductive response to hypothetical or real sequences of recorded rainfall. This approach is based on the successful application of 'vital attributes' in secondary succession modelling to predÍct the composition of disturbance-prone vegetation subjected to fires or other disturbances at varying freguencies (Nob1e & Slatyer L979,1981). In application to the reproductive patterns of arid zone perennials, the approach would focus attention on the mechanistic basis of plant reproduction, the significance of adaptive sets of linked traÍts, and the types of climatic seguences on which plant reproductive strategies depend in the arid zone. ÀPPENDIX 1 ÀNÀLYSIS OF MISTLETOE DISTRIBUTION ÀCROSS HOSTS I collected data on the number of mistletoes of ômvema SJgDdang per myall (Y) and the height (Xr ) and maximum canopy width (Xz) of each tree during fieldwork in November-December 1981 (sectÍon 3.1): Y = 5.53 mistletoes tree{ n = 85 western myalls sampled s2 = 84.28 (variance of Y) The data did not fit a spatial Poisson distribution (Table À1.1), thus mistletoes were not distributed independently of each other across potential hosts. The large value of the coefficient of dispersion (s2 lY = 15.2) indicated a high degree of contagion in mistletoe distribution. The greatest departure between obsen¡ed and expected frequencies occuffed in both tails of the distribution, i.e. signíficantly Iarge nu¡nbers of western myalls $rere parasitised by no mistletoes and by many mistletoes. Table À1.1 Comparison of observed and expected Poisson frequencies of Y. No. of mistletoes per tree 01234567-910-15t6+ 0bserved 27 13 5 6545 6 6 8 Expected 0.34 1,.87 5.16 9. s0 13 ,74 74. 53 13. 39 7 .31 0.41 0.01 x2 =8636.4x**,9d_f_ Margaret Ìlorris and Dr lù,N. Venables, Department of Statistics, University of Àdelaide, modelled the extra-Poisson variation in the data-set, using tree dimensions as covaríates. The model of best fit was based on the Negative Binomial (NB) distribution, which assumes that plants are distributed in clusters and that the number of plants per cluster Page 283 follows a logarithmic dÍstribution (Greig-Smith 1983). Given the mean number of clusters per tree, !, and the mean number of mistletoes per cluster, e'/a, ! is distributed according to Y ¡ NB(L/a, e*) which is equivalent to Y^/ NB(t, t/t(t + exp(X))) s¡here t = L,/a and exp([) - t(e' - 7)/a Morris & Venables assumed that the mean number of clusters per tree took the form L = exp(M) (which ensures that ! > 0) and found that the model of best fit was l,l = þ¡ + brXr + bzXz + b¡Xz2 The canopy width-squared term was sigmifícant, and had biological meaning insofar as mistletoe density was presumably related to canopy area. The maximum likelihood estimates for the model were Estimate S.E. t 0. 676 0.089 b -1. 515 0.780 b1 0. 467 0.20s b, 0. 197 0.081 b. -0 092 0.029 A X3 analysis of the observed and expected values based on the model yietded a non-sigrnificant result (Table A7.2>. Thus, the Negative Binomial distribution adequately described the contagious distribution of Amvgma quandang across western myalls. Page 284 Table À1.2 Comparison of obsen¡ed and expected Negative Binomial freguencies of l. Two of the 85 myalls were not scored for canopy dimensions. No. of mistletoes per tree 0 1 2 3 4 5 6 7-9 10-15 16+ 27 t2 5 5 54 5668 26.58 11.80 7.63 5.55 4.28 3. 42 2 .79 5.99 6.43 7.50 f = 2.986 NS, 9 d.f- ÀPPENDIX 2 THE BIRD COI'ÍMIJNITY Bird observations in the study area and elsewhere on Ì'liddleback and Roopena stations s¡ere recorded every 1-3 d during fieldwork between 1980-84. I made notes on the abundance and habitat of all species. The data permitted species to be classified in one of the foJ.lowing categories:- Resident (R): species continuously present in the study area. Local nomad (L): continuously present on the station or in the region but not in study area habitats. Often resÍdent in habitats (e.g- shrub steppe, disturbed habiLats) near the study area. Nomad (N): occurred in the reqion frequently (at least every 72-24 mo) but in an aseasoneil pattern. Migrrant (M): seasonal visitor to the region in most or all years. Vagrant (V): infrequent or rare visitor to the region in small numbers. Quantitative data on bird abundance were obtained from censuses over a 3 yr period between August 1980-JuIy 1983. The methods are described in section 5.2.2. À11 species recorded during the 38 censuses are listed in the table on the following pages. The data are the freguency with which each species $¡as recorded (percentage of censuses recorded) and the mean nunber of birds per census. Species are classified as residents, Iocal nomads, gþ- according to the criteria above. Vernacular and scientific names follow the Royal Àustralasian Ornithologists' Union (1978). Page 286 Species Freguency Months in No. of Status (ot") which birds/census recorded 1 (range) 7 Emu 3 IX .03 (0-1 ) L Dtqmaius ¡gveehol lqndlee 2. Collared sparrowhawk 5 II,XI .05 (0-1 ) L Àcclpitel qlrrhecephalus 3. f'ledge-tailed eagle 3 II .03 (0-1 ) L AquiIa audax 4. Brown falcon 3 XII .03 (0-1) M Eelqg beriqora 5. Àustralian kestrel 13 IX-XI .26 (0-3) L Falco cenchroideg 6. LittIe button-quail 3 I .03 (0-1 ) H Turnix velox 7. Common bronzewing 27 I,II,VI,VII .47 (0-6) R Phaps chglcsptera IX,XI ,XI I 8. Crested pigeon 34 I-IV, VI-IX .95 (0-5) L 0cyphaps lophotes XI,XI I 9. Galah 34 r, rv,vl-xII 4.53 (0-55) L Cacatua roseicapille 10. Purple-crowned lorikeet 3 V .11 (0-4) N Çlossopsitte pomhyrocephela 11. Budgerigar 3 ÏX .08 (0-3) M tfelopsittacus undgþlus 12. Port Lincoln ringrneck 13 VI,VIII, IX,XI .26 (0-3) L Barnardius zonarius 13. Mulga parot 42 I-IV,VI-Xrr 1.66 (0-15) L Psephotus vagius 14. BIue bonnet 32 III,IV,VI .95 (0-8) L Nerthie I le ¡eemalÞo-gester IX-XI I 15. Blue-wirqed parrot 5 III, IX .11 (O-3) N Neophems ghryggglgne 16. Black-eared cuckoo 24 III,V-IX .42 (0-3) N Chrvsococcyx osculang 17. Horsf ield's bronze-cuckoo 13 VI I I-X .21 (0-2) r,l Çhrygggocgyt þeEqIis 18 . l{elcome swal low Lt IV,VIII, IX .32 (0-8) L HfgUlde neexcne Paqe 287 Species Frequency l'lonths in No. of Status (r.) ç¡hich birds/census recorded 1 (range) 19. Tree martin 5 VI.XI .05 (0-2) N Cecropis niEeiqe¡S 20. Richard's pipit 11 I,III,VIII, .11 (0-1) L Ànlhus novaeseelandiae XI 21. Black-faced cuckoo-shrike 37 I,II,IV, .68 (0-5) L Corac ina novaehol larrlige IX-XII 22. Red-capped robin 82 r-xrr 1.82 (0-5) R Petroica qoodenovii 23. Hooded robin 3 III .08 (0-3) L Helanodrvas cucul.La!a 24. Jacky winter 13 III,VIII-X .24 (0-3) L Hicroeca leucophqea 25. Rufous whistler 76 IV, VI I ,VI I I .24 (0-?) R Pachvcephala ruf iventris x-XI I 26. Grey shrike-thrush 34 II-IV,VII-XI .47 (0-?) R Cg!þr i c rng.Le harmo¡n :!ca 27. Crested bellbird 37 II-IV,VI,VII .55 (0-3) R Qreoica E¡lturqlis IX-XI 28. S¡ilIie wagtail 5 I Ix .77 (0-3) L Rhipidura leucopþry9 29. lJhite-browed babbler 97 r-xrr 70.82 (0-25) R Pomgtostomus supefc:LLlosug 30. Variegated fairywren 7T I-IV,VI-XII 3.34 (0-10) R I'lalurus lgsþeÉi 31. tlhite-winged fairprren 37 I-III,VI-XII 1.21 (0-8) R Halurug leucopterus 32. Thick-billed gnass$ren 5 III,X .05 (0-2) L AmvlqEnrg !ext!Ii-s 33. Redthroat 32 I-IV,VI,VIII .42 (0-3) R gericornis þrunneug XI,XII 34. Inland thornbill 95 r-xrr 3.61 (0-8) R Àcanthiza apicalig 35. Chestnut-nrmped thornbilL 87 I-XI 4.47 (0-15) R Acg¡lhizg uropvqialig 36 . Ye I low-nmped thornbi I I 67 I,II,IV, 3.87 (0-20) R ÀcanthÍza chrvsorrhoa VI-XI I 37. Southern whiteface 39 I,III - IV, .95 (0-4) R òphelogepþqlq leucoPsig VIII,IX, XI,XII Page 288 Species Frequency üonths in No. of Status (r") r¡hich birds/census recorded X (range) 38. Varied sittella I III, IV, IX .32 (0-6) L pgpþenosttle chrreqlere 39. Red wattlebird 34 III,IV,VI-X .61 (0-3) L Ànthochaera carunculata XII 40. Spiny-cheeked honeyeater 100 r-xr r 23.16 ( 5-47) R Acantbaqenvs nrf oqularis 41. Yellow-throated miner 26 T,ÎT,IV, 1.82 (0-21) L Manqrina flaviqula VI I I_X ,XI I 42. Sinqing honeyeater 97 r-xrr 5.92(0-77) R Lichenostomus virescens 43. White-fronted honeyeater 18 II,IV,VIII .42 (0-7) N Phvl idonyrÍs albi ffqng IX,XI I 44. tlhite-fronted chat 13 IV,VI,VIII, .66 (0-14) N Ephthianura a!þifrong X,XI 45. Mistletoebird 87 r-xrr 2.84 (0-8) R Qicaeum hlfUndinecCuE 46. Yeltow-nrmped pardalote 5 v,xII .05 (0-1) l,f PaEdqþtus xanlhopyzug 47. Silvereye 3 IV .03 (0-1 ) N losteropg lateralis 48. Zebra finch 3 II .11 (0-4) v Poephila crutteta 49. Common starlinq tt VII,IX,XI .29 (0-5) L Stgrnug vulqaris 50. Black-faced woodswallow 3 IX .11 (0-4) L ArLaSus cineEeus 51. Dusky woods$rallos¡ I VT I I-X .16 (0-3) N Àflamgg cvanopterqg 52. Grey butcherbird 68 r-xrr 1,29 (O-7> R Cracticus torquatust 53. Australian magPie 34 I-III 1.00 (0-8) R Gvmnorhing tibicen VI I-XI I 54. Àustral.ian raven 63 rI-X,XII 1.55 (0-9) R Coryus qoronoides 55. Little raven 5 III, IV .37 (O-11 ) N Çgr.¿Ue mellori 56. Little crow 8 III, IV,VI .45 (0-13) N Corvr¡s bennetti Page 289 ÀPPENDIX 3 ÀNÀLYSES OF VÀRIANCE - ORIGINÀL DÀTÀ ÀND TÀBLES 3.1 HAND-POLLINATION OF 2_10 d OLD FLOþIERS (REfEr TAbIES 6.6 & 6.7) t lol len crrains adherinq/adjacent to stiqmatig:api I lae Original data FLOIITREA : treatments - short (SXO) and long (LXO) cross-pollinated; self-pollination (S0); autogamy (À0); ancl controls (C0). PROPG : proportion of styles wÍth pollen grains adhering/adjacent to stigmatic papillae. NOPG : mean no. of pollen grrains adhering/adjacent to stigmatic mPi Ilae. SSIZE : no. of replicate styles examined per treatment and plant. * : missing values (no old flowers available for experimentation ) FLOUIRfA P RO9 PO NOPG s sr ? É PLANl q BT sxo t a 0 36 6l Lxn 1 a {) 22 I B B1 so 1 a 0 ?6 0 a 4 ô 5 å:. q 81 0 a 6 co^o { q Ð2 sx o 0 a ô 57 e2 LxO 1 a 0 2Z t g2 sa L a I 5ô 5 ¡2 lo o a 6 13 5 q2 cîl 0 a 6 I ã EI sxo o a 6 29 5 B3 LXO 0 a ô 1i s â3 SO o a ô 66 5 R3 o a 6 4 5 'ro q 6 B3 co o a ô 6 B' SID 1 a o 1f o a 6 ôt ã ¡ô Lxn q 8a 5fl 0 a ô 1t Ð4 AO o a ô 41 5 B4 co o a 6 9 ã 85 sxo a a a it LXO Or c 11 q Bã so 0¡ ô 5 a "0¡¡ I tt AO q B' co 1 a 0 2L 06 o a 0 '1, 5 -sx t j B6 LXO o a ô t2 a6 5(l o a ô ct 5 AO o a 2 2 5 i6 q B6 co o a 6 2t rl sxo o a a t ã UÕ Lxn o a 6 t6 ã Y' so 0 a I i s YÔ Ao o a 4 2 5 YÕ co 0 a 0 0 ã r5 5XO 0 a 7 1,t 3 Y' LXo L a 0 ¡a ã T6 so o a 6 ô 5 Y, AO t a o I 2 vt co o a c 2L 5 Page 290 Anova tables Variate : angular transf ormation Iog transformation of of PR0PG (NoPG + 1 ) Source of d.f- M.s. Source of d.f. Ì,f.s. variation variation Plants 7 .2416 Plants 7 7.2807 Treatments 4 .1852 NS Treatments 4 4.3724x* Residual 26 .1725 Residual 26 .71 00 2. Pqlten tubes penetrglinq between st:Lcma'b:Lc Dapillae Original data - abbreviations as in 1. except: PROPPT : proportion of styles with pollen tubes penetrating stigmatic tissue NOPT : mean no. of pollen tubes penetrating stigrmatic tissue Sample sizes as in 1. PLÊNÏ FLOUTREA PPOPPT I{OFT 9.1 sx0 0.8 t2 Ê! LX0 Ð.Ð 13 gt s0 t-ø 2ø Ê1 AÐ 8.4 4 Bf c0 È. { s EE 9rX 0 Ð. b' 29 Þt-A4 LX0 1. g I ßr't s0 0.6 I 9bG'} AO 0,4 t a? c0 a.2 I 83 sx0 0.6 1L _ Êi LX0 Ð.4 t3 E3 90 rl. ê 64 v, Êr] tl. r5 h E3 c0 ø.8 a e4 Ëx0 Ð.8 t{ Ê+ LX0 r¡. r5 î,7 E4 s0 8.+ 7 gi Ê0 0.8 5 e4 c0 0.6 -389 s5 sx0 r¡. I e5 LX0 ø.4 22 e5 s0 rt. B 66 et AO 0.0 0 e5 c0 l). { t5 6,5 9X0 t. lt E5 L¡(O 0.6 6 ett s0 0.6 ,52 EÞ' AO û 'i 8¡; c0 ø.8 tÐ U¿ sx0 Ð. ,t ¿8 tì4 LX0 t.6 l6 ,' ulî 90 0.6 I r{4 Ê0 e . ¡t I ' hl4 c0 ø.9 Ð It5 sx0 ø.î 4 U5 LX0 t.0 3'1 g5 s0 4.6 3 H5 â0 ø.e g t5 c0 0.8 t8 Page 291 Ànova tables Variate : angular transf ormation Iog transformation of of PROPPT (NoPT + 1 ) Sowce of d. f . M.s. Source of d.f. tf.s. variation variation Plants 7 .0885 PIants 7 .6938 Treatments 4 .3164 Ns Treatments 4 6 .0624*** Residual 26 .7178 Residual 26 .78i3 3 Poffen tUbes_reaghi Dq-glyfsE-Deqh 0riginal data : abbreviations as in 1. except: PROPPT : proportion of po1len tubes reaching stylar neck NOPT : mean no. of pollen tubes reaching stylar neck Sample sizes as in 1. FLå Nr FLÐUTREÊ PRO PPT N0P T Þ-r s,( 0 tÐ- I 6 Or L'( Ð tâ-t 7 Êi. s0 r.0 t ? ÙL f{0 {r- 2 2 E-Í c0 0. ¡l 5 sx0 rl- 2 ? e, .7, LX0 0.6 2 s0 0.2 0 È') .40 Ð.2 o 82 c0 Ð. B o 83 sx0 0.2 I e3 LX0 0.e L Þ3 s0 g.g 1 ø B3 AO û.6 3 83 c0 9.6 I 94 . sxo t.? I 8{ LXO å- 6 1 e{ s0 a.o o B4 Ê0 0.6 2 P¡ c0 o.6 3 0) sN0 * + Ê5 LX0 ø. ?. 0 85 s0 e .6 7 e5 AO |t t ClF c0 0.6 1 eri tx0 e.6 5 86 LX0 0. { I It s0 ø.6 5 e6 AO e .0 0 Et c0 e.2 { U4 sx0 e.2 I g4 LX0 0.8 0 rd{ s0 0.0 e !¡4 RO a.2 0 U¡ c0 e .0 0 95 sx0 e.c 0 r¡t LX0 t. e I ct s0 9.2 e U5 â0 0.e 0 rr5 c0 e .8 { Page 292 Anova tables Variate : angular transf ormation log transformation of of PROPPT (NoPT + 1) Source of ùL ì,f .s. Source of dJ- ì,f .s. variation variation PLants 7 .0885 PIants 7 .6938 Treatments 4 .3164 NS Treatments 4 6.0624.'f** Residual 26 .t778 Residual 26 .7893 4. lenetrallen_qf pollen_lubgg-þCyqnd_styleq_¡eck Original data : abbreviations as in 1. except: PROPPT : proportion of pollen tubes prenetrating beyond stylar neck DIST : mean no. of stigma lengths beyond stylar neck penetrated by the furthest pollen tube. Sample sizes as in 1. PLriHr FL']UTREÉ PRO PPT D I s T g1 sxÛ s. g 3 g: LX0 0.2 1 s0 0.8 3 Ê'! Ê0 9.2 1 EI cÛ t.4 3 Pî. s¡( 0 ø.2 ø 8¿ LX0 0.6 1 P¿ 80 9.2 1 Q't â0 ø.2 0 83 c0 o.0 e 83 sx0 ø.2 I g-3 LX0 0,î a ei s0 e ,I 3 êt Ê0 ø.6 I e3 c0 0.6 I 8{ sx0 ø.¿ o g4 LX0 Ð.6 e 84 s0 0.0 6 e4 ñ0 0.6 I e4 c0 -t9.6 t Ë5 sx0 ¡¡ 05 LX0 ø.2 g e5 t0 tr. 6 t D5 AO a I 05 c0 0.6 3 à;. sx0 0.6 I 8o: LX0 e . ¡1 e ái¿ s0 Ð.6 0 s; RO e .0 e ET c0 ø.2 0 u4 sx0 g.z 0 l, .¡ L¡( O e.0 0 u4 s0 0.0 ¡ lr¡ ¡ ñ0 4.2 0 U{ c0 0.e 0 gt 3X0 c. e -,3c u: LX0 l. a ui s0 a.2 c U5 RO 0.0 0 a1 c0 3.8 2 Anova tables Page 293 Variate : angular transf ormation Iog transformation of of PR0PPT (NoPT + 1) Source of d.f. M.S Source of d.f- M.S variation variation Plants 7 .1828 PIants 7 .5947 Treatments 4 .0488 NS Treatments 4 .1790 NS Residual 26 .t7t2 Residual 26 .2t70 3 ,2 1981 & 1983 EXPERIMENTS UEÀSURING SEED SET ÀFTER HÂND-POLLINATION (Refer Table 6.9) 1 . June:Jqly-dateJ9Sl cxPcelment Original data FLOTJTREÀ: treatments - control (c0); autogamy (Au); long (XL) and short (XS) cross-pollinated; and self-pollinated (SE). Y the number of young fruits per branch in June-July. N the number of flowers turned over by June-July. PROPN Y/N T the angular transformation of (Y/N) tf missing values, branches used for apomixis treatment. pt{ PLANT FLOUfRg A Y N P FO T 6¡6 co 1t1 339 o. Õ4 5+ 0¡7307 Br6 AU 16 2'r 6 O¡0!!0 0¡2132 6¡ 6 XL 5 118 Or0l1? 0¡220Ò 6¡!i xs 1 11Ò 0¡0Ott 0o0939 8¡6 sg 2 1ô6 0. 013? Oettt! 31¡ 1 co 1C0 !62 Oo5OE3 O¡793? 31r 1 AU a .a a 'rf 31. 1 XL 6 t2 o.t1tl 0.3¡6 i t1o 1 xs + 1t O o2222 o ¡{00 I 31¡ 1 SE ? t? 0o0t0l 0 c 2l'l 7 t1¡2 co 2t3 35r 0¡?O6? o o 0l t 5 31¡ 2 AU 1 ,2 0¡0192 Þ ¡1390 31¡ 2 XL I t3 0ot,69C 0 .124? 31¡ 2 xs t'l ?t 0r21"9 0 oltã7 31¡ 2 SE 13 t2 O¡1lL3 o ¡!Cã1 6.21 co 503 a2'l 0. ?o gE 1 r 001? 6.21 AU a t¡ a a C.21 XL .1 a? Or02lt 0 o !l8l 3 o21 xs 1 ,, 0o01i2 0 o1Sã3 G.2t SE ô 19t Oo0l0t Oo2024 31¡ 3 co 1?3 ô05 o. a272 Oo?12! tlo 3 AU 1 100 0o0016 0¡0?19 31o 3 XL Ò t3 0o0?95 0o2?ll !1¡ t xs 0 tl Oe0000 0.000 0 51o 3 SE t 1at O¡0tO! Ot2Q2 1 C o2Ò co 2!e tt1 0.6t0¡ 0 r C?0 , C¡2f AU t¡ t¡ a a lo2ô IL 11 124 Oo0t?.1 0 o 2ti t t¡2Ô x5 , 11t 0o0120 0 ¡20 lt ô C o2Ô SE ¡ 'tc 0¡11ãl 0 o tlt ¡ G o2J co 2l o 302 Oo tlll o o tl e 1 C¡21 AU 1 i a1 0.20t9 0 . Õ?5 ¡ C o2J XL 2 2 10a 0¡ 2O !7 0 . ¡t I t 3o23 xs a a z'r, 0o232? 0 oã0t Ò 4.2, 5E t ¡ 1¡t O¡ 2!e I 0 oãO?? 3 ot1 co t1 ô a?1 Oo33t? o ¡Cl5l C¡11 AU a a 'a a t¡11 XL 2 aa 0o 0tt! 0 o !?? I 3o11 xs t 1"? O r 0{t2 0 ¡2tô2 a.1l SE a 11. 0o0t?l 0 ¡21!t Page 294 Anova table (Variate,T) Source of d.f. M.S variation Plants 7 .t6742 Treatments 4 .63007*** Residual 24 .01065 2 Lele_EgBlenþer da!a-_!981 experimgnt Original data - abbreviations as in 1. except: Y: the number of young fruits per branch in late September N: the number of flowers turned over by late September PLAilT FLOUlREA r N P FO PTI 1 31o 2 co 250 la1 0r 6 t6 20 o o9l a2B t1¡ 2 XL t1 ô1 0¡ 15ãr0 o ¡3? ?{1 !t¡2 xs 2l L2C O¡ t t410 o ¡11?o c t1¡2 SE 1.' to6 O¡ 1 12tO o ¡ 3? t9? 6.21 eo 2't 3 t4a O¡ 501r0 o ¡16tzo 5.21 XL 2 63 O¡ 0t1"0 o ot? 900 6o21 xs o t1 0o 00000 0 ¡0000O | ¡21 se 1 20t Oo o0a09 o ¡07096 51o 3 co t?1 10t¡ Oo 35200 0 .8 3tt t 31e t XL 2 119 0r o1120 o ¡1 0603 51o 3 xs 0 13? o; 00000 o oO 0000 t1¡ t SF 5 911 0¡ 01610 0 ¡1 2423 f¡2ô co 13t s tt 0¡ a2a70 0 ¡7 ta6 6 t ¡2t XL 6 1r5 0o 0t240 0 ¡t coÐ 9 to2ô xs 9 1+6 O¡ o6160 0 ¡2 ãoc 1 to2ó SE 10 111 0¡ o 9010 0 rS 0aô ? C o25 co 2G3 391 O¡ 6?2ñ0 o ¡9 616 2 3 o2) XL 1t 1!ô O¡ 1!a50 0 .trt?1 3 o25 xs 29 29Ô 0¡ o 9i 60 o o!tll1 3 o2i SE + 2L'l 0¡ o1ôÕo o o1tõ07 Ànova table (Variate, T) Source of d-f. M.S variation PIants 4 .066447 Treatments 3 .443522*xx ResÍdual 72 .007363 Page 295 3 1983 Expesiment OrigÍnal data - a.bbreviations as in 1. except: Y: the number of young fruits remaining ín November from the experimental period N: the number of flowers turned over during the experiment *: missing values, no flowers available for experimentation PLANl FLOU TRE A Y tl PROPN 1 B1 c o 89 ¡0 0¡?66"0 1r068"1 81 U 1S t0 0o20O0O o. a636t ;1 ^x L l1 c2 0o1??40 Ool3ô"6 81 xs 20 60 0.3 33 30 O¡ 6 15aa B1 SE 9 65 O¡1tt50 0.3 ô13 3 B2 co 1a 6¡ 0o20290 O¡Ò 6'?26 B2 At, o 4 O¡00000 O¡O 0000 B2 XL :, 1r 0r0ã560 O¡2 tr 0 a g2 xs o 29 O¡O00OO OrO 0000 È2 SE 14 0r2?ô50 O¡5 51ô 6 B3 CD 3 'L30 O¡10000 0¡3 ?L't 5 8t AU t ôa 0¡022?0 O¡ 1 tt2+ Bt XL o 21 0r00O0O Oo0 0000 Ð3 xs o 16 o.00000 O¡O oo0 0 t3 SE o t6 o.o0o00 0¡0 0000 B4 co 1t 26 0¡6e2!O Or9 c21 e ¡l AU g ?3 o.12330 Oo3 5t79 B' XL i 20 0oa0o00 Oo6 ãlr 2 B¡ xs z tz O¡1t6?O O¡l 20' rt rô SE 2,'l ,6 Oo30360 O¡5 ttt 6 B' co ôo 'r6 0¡ã2630 O¡! 117 1 g, AU 1 20 0¡0!000 0o2 2r)l B' XL o ? 0¡00000 0¡O 0000 It xs 2 10 O¡20000 0¡ô 636t à, SE 10 3? 0¡2C360 O¡5 615 0 BB co 3t ó6 O¡7601O 1¡ O 59 t a 88 AU 26 aô 0 ¡ ã 90 e O O¡f ?6t1 B6 XL a a a a 8e xs a o a a t¡6 SE 10 25 0.100 o0 o.ttl"2 ta co ?G to Oolltt0 1¡16ã31 vÒ AU 0 1r 0eO0O0O O¡00000 U' XL , 1? 0o2¡110 0. t?tt I vÒ x5 a t0 0¡1!t30 0ot?!?ô UI SE a aa OrO67ô0 O¡ 2 6!ô2 U' co at ,a 0. t t6 ¡0 1o2!OOl vt At, !c t1 O¡!tllt0 o.tt022 a, XL 11 1ô e.atat0 Ootl!lt Y' xs Ò et O.1?!t0 0¡ô!011 U' SE 22 ¡ll 0¡ô5tt0 0.?ôt6t Anova table (Variate, T) Source of d. f- l.f. s variation PIants 7 .29890 Treatments 4 .395041(** Residual 26 .03539 3.3 NECTÀR STANDING CROP üEÀSUREI'ÍENTS (Refer Table 6.10) Page 296 7 19s1 Original data FLORÀLPH : f loral phases, maJ.e, intermediate and female MGSUG : floral nectar content (¡9 sugar/flower) F¡. 1=gQRT(MGSUG+.5) FLORALPH ¡1 65rtG 1 r,AL E ,-l I 23¡96ô73 r NT€ PX 0 O¡?0?11 HALE jt 723 4l¡5.1 ã06 INTEFT{ 100 l0oO2{q? }IAL E L72 3 41.51ã06 Il"llERt{ ?-25 15o01666 I.I ALE 1053 3Zt4Fr65 INTERII ñc I 2_6.2-5â3.1 ttALE 960 30o99193 I{IERH 100 10.02497 IIAL E af,1 1lr 6 47ít 2 ¡ r¡T ErrH 99ß 30 ¡ 6 O229 TlAL E 2t4 llo l^5i2 INTFo¡. 46 6 21.61^â6 XAL E 94 a.72 111 rNlEPl{ 3c4F 6¿.01210 H AL€ 103 t 32.2251'l ¡NT€Ri{ 9r6 31.40ô60 I{ALE 239 15.34601 ¡ NÏERH 99r 31¡ 59905 HAL E 235,. L5.34601 TNTEQH â7'l ?6r02â;3 { ALE 50¿ 2trSt13? rNf E q¡l 1i ? 13.69306 I,IALE 10 0 10. 0 2a g'l rN l EftH E6 0 23o6?4 li H ALE 1?96 42.3ô514 INTERÈ{ .lô ô 19.71040 i,tALE zoo 14¡159t0 fNTERT'l 3ô 2 19.51"61 HAL € too 1Or 02ô97 INlEEt. ?92 t7 ¡ 102 63 TALE t+0 1t.4f264 l NTER¡' tf01 110436õ1 iIAL E ¡9ó 1 9¡ â 6ZO2 INTERr. 1ôr5 430 42214 H ALE t 123 33¡51t65 ¡NTERI¡ 149? 3e ¡ 697F5 1.¡ALE 663 25.7Ft49 rNTE Pr'l I2L¿ 3ôr 9O7O2 iIALE 95 ? 30o 94350 INlE E !. c?- t 30040'170 IIALE zt50 Õ6.3ttlt INT ERH L244 36.2a?+a t.ALE 23f i 4c¡ â?220 fNTERrl 'rLt 2 6. ?l 1¿2 I,I ALE Lg't z 44r 412 C4 rNTERrl 112 9 33r60605 I,IAL E 139C 3?r396Fz INlEPH 1360 3ll¡ CËô9ß IIALE 191 1 43.720.'O If,¡lEPLf 11ß 1 34o0â0?e r{ALE 100 10¡02tt? INTEF X 9"5 .1 1.23300 r.{ ÀLE 100 10¡ 0249, fNTEPI¡ 936 30. 6 02"-g i4ALE 100 10r 0249 7 rNlEex 115 4 35r6ô23ô rALE 100 10¡02497 Ir{1Ë R ll 560 23¡ 67ót t HALE 100 10.0249? TNlEPH 100 LA . O24 97 I't E 305 t?r 47t s 6 I NTERM e05 10.09153 IIILF^L 93ß 30.6O2.29 I NÎ EFH 100 10r0249? H ALE ,a2 29.?05q0 r NIERII o 0. ?0711 HALE 1"3 9 41.?Q?31 r HTÉR H A3t 2A ¡ 9 4O.1 S FAL E 12q 6 35.4ô?1ô TNlENT 100 lOr 024e7 HALE Ðo 2 S0o0+18t ¡tlrEFr' 20tA 4ã.2161F HAL E t9i 29¡ 97499 TNTERI{ o 0¡?0?11 r.ALE ño 9 ?-4.6ttoã I NlERI¡ ctô 26¡5J9i5 }IALE L59 2 39.00614 FE¡'ALE 662 29056t-tá I{AL E ztf 9 52. ô3567 FEHALE ã74 23¡ Ðt C?3 XAL E eL?. 2i¡f0+39 FEH AL E 229 À 4"¡9126? HALE o 0.70?11 FEIl ALE 139 4 3?¡ 34300 H ALE ù o.70?11 FET¡IAL E 100 2 t1.6 622C i.ALE o Or7O711 Fe rALE 114 9 3.1 .90ô2ô HAL E o 0¡?0?11 FElr^LE 736 2?.1¡t53 r{ALE 160I l0¡ Qi11? FET'ALE 401 22.16 S D 0 TALE 2016 44.90t48 FEF AL E 1413 3?r 59654 tlALE 0 g. f e"11 FEltlAL E 100 1Or02a9l rALE 6'12 25.93260 FE}IALE ã10 22 t 5t 421 IlALE o O¡ 7O ?ll FEHAL E 1t9 13¡3¡"76 rAL E t9I 22cÐ1910 FE l{ ALE 14{ 12¡Q20i2 rALã 2069 45.4Ðl-t6 F EHAL E 119 10..t3161 FALE Tzr 22. Q 363t É EHAL E 903 22.a3ôCl rlALF 2t4 14¡64662 FEU AL E ?ti llrô+tô5 HAL E 100 10.02r97 FêI{ALE 32L 22. i3 63" r.ALg t04 1q¡ â6202 FEI'ALE too 1O¡O2Ô9? ¡NlEPt' 3592 5!1 .9 -l-tL13'l a'l FETIALE 3 3'l lâo37117 ¡NTEEF 2Eô Llt2 FEl,l AL E 164 :1 20 C2â"6 ¡NTEPtl 36 t 19r 1 963q FEF TLE o o.?QatL tNT ERH 6ñt 25 o'l 196å FErlALE 0 0.?o?11 I NTEer' tr0 e l0¡ ô 6 42.2 FEH ALE 20c tf ¡ 47a11 ¡NlqRH 100 10.0 2.91 FEI,I ALE o o.?0"11 tÈTEe r 100 10rO 249? FãHALE 100 10.0¿ô97 TNTEEH 10 0 1O¡ O 2491 FEIIAL E ^t6? 19¡1"029 INlERIl 100 1Oo 0 219? FEHALE 100 10.0219'l r1{TEAH 20 s ll¡ I 7ôt 1 FEIIAL E 100 10.02+9? lHlECtl 3r2 l,to? ?¡90 FEH AL E 100 10¡02t97 1^¡ 1E PH 396 19¡ 9 6 2ô 6 FEHAL E r00 10¡ 02r9? INT ERH 100 1Or0 2_4t7 FE" ALE 100 10r 02a97 TNlERU 100 10. 0 2¡97 F€ ¡'AL € ?oã 26.9512t Page 297 FE r.AL E L2-tr 6 35r ô6"i1 FE X ALE ttc 2âc 2 6 15 6 F E¡IAL € 360 t'r9l6l¡ FEX AL E ß 6.3 25 .7 5t49 FEH ALE 100 lO¡0219t FEl,lAL E 100 !0o 0 2491 FEII ALE 2044 45.2161F FEftI AL E 100 10r O 24 9-l FEtl âLE ZLL'? 46.01610 FEH ALE 100 10¡0 249'l FEIIALE 2q9 lt¡3 0607 FE¡IALE 292 1?o 1 02G3 FE{ AL E 69? 26¡41023 FEf.t AL E 0 0¡? 071 1 FEUALE l6+{ {O ¡ 5 5?4 4 FEI,|ALE 100 10o 0 2ó9" FEr.ALE 1ro3 36r1 0402 FEX AL E 100 10r 0 ¿49" FET4ALE f,5 6 2q.2 6602 F5{ ¡LE o 0. ? 0"11 ÉEFALE t9Li 4.3¡ t 006a FEIIALE 0 0.? o 111 FEII AL E 214'l 49.1 't 22L FEÈ' ALE o 0¡7 o?11 FEI{ALE 938 30o 6 o229 FET,IAL E 100 10o0 2+97 FE¡IALE 100 10¡ 0 249" FEHAL E 6ã1 25c5. 245 0 FEHALE 100 10¡ 0 24at FE HALE o Oo7 0?11 FEIALE 3'r, 11.3 2ñ15 FEl'l ALE 100 10.0 ¿40? FEI{ALE 0 0r? 0711 FEI,IAL E 100 1Or 0 2\ 9? FE!'AL E 100 lo.0 2197 FEMAL E 93ô 50. F 6S59 FE{ ALE 1t ? 13o 6 9306 FÉ,r{ALE 72¿ 2 l5¡ | 1201 q3 FEHAL F ?t0 21 .g 3 743 FÛTlAL ç ô 3O ¡ 5 6Ç9e FEII AL E o O¡ ? 0 ?11 FEHâLE 93t 3D¡ 5 6959 FE F ALE 0 0¡7 o 711 F Er¡iALE 5ô9 23¡ A 4142 F SHAL E 100 !0¡O 2+9'l FEl.lAL E o O.? o ?11 FEI'AL E 903 30¡ 0 ,à26 FEIlALE 0 0r ? 0 FgHAL E f,56 29. Z 6602 "11 Anova table (Variate, T) Source of LL, H.S variation FIoraI phase 2 640.7x Residual 188 787.4 2 L292 Original data - abbreviations as for 1. F LORALÞH PASU O 1 l,l ¡ LE 29I ta r30G01 H ALE ô46 ?1 ¡13055 II ALE 0 o r ?0 711 M ALE 59 4 2.4 .3â237 IIALF 29 9 It ¡ 30G0? 14ALE ¡ô6 ?l ¡13055 HALE ôåt 2L tt1 'tt?. .{ALE ¡ô1 23 .2t011 I.IALE 62ô ¿4 r f 8O0O T{AL E ãèt 23 o27015 HALE 624 2i ¡ 99OOO ilAL E 5r1 2t o 2'lQLâ t4ALÉ iL2 T7 .6776? r.r ALE ß70 25 . â9ôO1 HALE l5 6 7,2 .51000 r.tA L E 1005 31 .?0962 r.lAL E 156 L2 .51000 L E t50r 3i ¡ ôt9ô1 I'rA LE 156 L2 ¡ ã1O0O '¡IA}.AL É, r!i{ 29 oZ t1+s I.IALE ô91 22 .169C0 I{ALE lL2 22. ¡5 3tl6 B HALE ò91 2?. ¡1 69ôO IIALg 3ô2 1t .J 06t6 HAL E ô91 ?-2 ¡1 ß I CO l.lALE 100 10 r0 219'l I,IALE 691 22 o1 69t0 tIALE 100 10 o0 249'l llAL E ¡t2 31 .t ôôâ6 r ALË, 100 t0 .0 2¡e? HAL E 1005 3t .'l 0s62 tlALE 100 10 ¡0 ?¿¡9? HTLE 1;4 3 42 ¡9 3600 I{ALE 125 0 65 ol' 95ô6 MALF 1Cô' 42 ¡9 3800 l,l AL Ë 4637 6t ¡O e91e ilALE c91 2g ¡ð Feoo ¡TAL E 1394 37 r1 ô300 XALE ll¡â ts .47ôñ3 ALE t 23e t5 ¡2 065t ¡{ALE 1ôâ õ It o F551'6 }'I" AL E 123 q 3B ¡2 0653 t{ Al- E ?-2 62 4'l .'l'l u52 IIALE 33 r3 5ôL6 t,IA L ã 276a 50 .6tOS? HAL E '-LL2222 7.4 ¡9 1643 XALF 3ô2a 5ît ¡91923 X ALË 1rt2 3t ._1 ã416 ilALE s4Ð2 5c ¡09?3â HAL E 1"ô O ôt r? 1e30 HALE 2149 46 ¡362?O }IALE c70 29 ¡5 oô2¡ I{ ALE 3ô92 9E .09?3ô HALE t21t 34 o9 0.t02 MAL': 99ô 31 ¡q990q t¡lALÊ 1e 1a a3 c7 5F00 t{ALE' 119t 34 .61916 HALF 2 97'l 5ô .q 664? I'IALF- 139¡ 3'l .30652 trtALt 2127 ô6 o1 2aE 3 Page 298 rIALE 916 30 o 2?3?5 FEHALE 20 6 H^LE r02 20.t2i¡3 FETIALE .10 9 I,|ALE 22E 15r14926 FE}IALE 4L2 14ALF 13"4 37.0?t25 FEHALE 61t HALE ¿72 0 32.L5ô41 FEHAL E 206 XALã ?-9 L l?¡ ù"t3? FEUALE e2l 2CL 17.0".3 l? FEt{ALE 0 '{AL€HALE 5r2 24.13B04 FEXALE 0 FEÈIALF 0 0r"0t11 FEt'IALF o FETALE 0 0.70711 FEi,lAL E 100 FEI'ALE 0 0.70r11, FEUALE 100 FET AL F o 0.70?t1 FET.TALE 100 FEI'I ILE 0 0. t0711 FE4 AL € o FEI{AL5 0 0r"0t1t FEHALE 0 FË HALE o 0. 70 FEI{ALE o FEtIALE 0 0. ?0 "ttttl FE I'I AL E 0 FEII AL E o 0. ttl FEI'ALE 0 FEI{ ALE o 0¡70?11"0 FE¡I AL E 100 905 30¡09153 FEHALE 100 FE{ALE o FE {AL E 905 30¡ 09153 FE$A L E FEX AL f,' e 0 5 ¡0r0915t FEHAL E 100 FEIIALE I05 30.09153 FE HALE o FEftlALE 905 30r09¡'53 FEX AL E o o FE f.{ A LE 129.t 36r 965?6 FET{ALE o FT¡H AL E ô65 2Loâ15a^ FEI'ALE FEH AL € o FE"IAL E 665 2L .57 Í 45 FEHILE ?ì3 L5t2ô071 FET'ALE o FEI.t AL E 2tl3 FEI.I AL E e33 15.2â0t1 AL FEiTALE 3994 FEH E ?.9I 16¡10900 2ã5 3 FEt{41.È F 1,7 22.t4C63 FEilALE FEHILE 1 141 FEHILE 29e 16.10000 29 FE tI ALE r?6 2ao A 69"5 FEHALE C'l AL E 2390 FEI' AL F 5'L'l 22.7 tô63 FEH F FEMAL E 2q I 16.1 0900 EMAL Ë Lr92 F ErlAL E ?-.t I o FEiI AL Ë, 403 2Oo 0 c 70t FËr.tAL E 26I 16 o 4 1648"31 FEX¡LE FEI,I A L E 0 0 ¡'l 0 711 FEttALE 2t20 FEIIALE ?0t FE*I A L€ 0 0¡? 0 ?11 'ro1 FEI'4ALE o 0¡? 0 111 F€ f'{ AL € FEI{AL€ ñ3c 2â.2 6r56 FEI.I AL E ?¿6 FE|.ALE 63â 2á.2 6ü56 FãTALE ¡41 FEXAL E 63â 25 . 2- 6 i5 6 FE14ALE 2L1 I FËHAL E t063 32tÈ1136 FEI4AL E r93? FEtIALE 0 FEI.IAL E L063 52o6 1r35 FEÈIALE s29 ,3o. ö tl'ro FEIl ALE ô3 ô FEI{ALE 43o1 1032 FE'.AL E 21S 1i5¡ 0 FEll Al- E 1r5t 43.1 t0l2 FEI¡IAL E F 36 ô FEM AL E 119 C 34¡ 6 1936 EHALç f,lA F EHAL E 7e9 28.2 ?FÔ3 FE L E 217 I FE¡' ALE 59I 24t\ ¡r69 FEÈIALE 49I FËT'ALE 100 1Or0 24 c? FE¡TALE 599 FEHALE 0 Or7 0 FE I{ ALE 119 C FE¡IAL E o 0.7 o?1"11 1 FEHALE 902 FE¡,IALE ?09 1?. t 060t FEHA L E Ito4 0 FEHAL E 299 1?o 3 0607 FEnAL€ o FEHALE ã 9.!r 2J.1 6ô26 FEt{ AL€ FE}IALE o Oo? 0"11 FEXALE o F 100 FEX AL E 200 1l¡ 1 59ôO FEH ^L 0 FEMA L E 100 10. 0 249? FEHALE Fêl'lAL E áL'' 22o 7 ôrt 53 FEI{ AL E 100 0 FEHAL Ê o 0r? o?1t. FEIlAL€ FEÈ'ALE 0 0.? o FEÈ{ALE o FEI.I ALE 219 16.1 0 "11900 FEM ALE 0 FEI{ALE 2.i e 16.1 0900 FEMAL E 0 FË}TALE 255 16¡1 0900 Anova table (Variate, T) Source of d-f* l,f.s variation FIoraI phase 7 7495.8*** Residual 787 240.4 Page 299 3.4 POLLINÀTOR EXCLUSION EXPERIMENTS - TOTAL SEED SET (Refer TAb]E 6.18) 1. 1991 Original data Treatments : control (CO); autogamy (ÀU); t cm mesh (CtJ) and 2 cm mesh (RM). Y : number of young fruit at the end of the flowering season. N : number of buds at beginning of the flowering seagon PROPN : Y/N T : angular transformation of Y/N * : missing value due to branch death P LAHT TREAT!{EN Y N P QO oÀl ? 31¡1 en -1 2 6 iqi 0 r.3 6'3 O1 0.6â66t 31¡1 AU 1" 19ô 0r08.'63 0 .3 00 5 t 31r 1 CY ßl 2¡9 0.19ß 9t 0 .ô59?i 31r1 PH 73 .3ô9 O¡1lt?66 ô ¡lÔi0A 31¡ 2 co 2âA 361 0 ¡ 6 561? 0 ¡ 9 4A-?,2 31r 2 2 ô1 O r O 2ô 69 0 r157t9 31. 2 ^t,,CY 52 160 o.32500 0 .6 0Ê Ê .|1 3tc?- Pt{ 49 tâ3 0¡26"?ô o o 5 ¡.1 ô tl¡11 co r19 537 0r5910¡ o ¡ ô â00 a 6¡11 AU a a a a 6¡11 c¡' 12 tô5 0r35ð62- o .6 ¿2 0 6 ß 6.11 P ?.t .?a 135 o.2cLbt 0 ¡5 E.¡ 2 ., 6¡12 co 105 3'l I ot?tl50 0 ¡5 59 ¿ ñ¡12 Att o â9 O. O 0|t 01 o ¡0 00 0 n 6¡12 cv l¡ t a a 6.12 eil a I a a 6.10 co toe 319 Or3lt69 0 6 21 3 z 6¡10 AU 17 1Ê1 0¡0919? o . .:l 1t 4 ô 6rtO cu l2 ?-'t o Or 0'ttl o t 212 t 1 G¡10 Frrl 61 ?- 33 Or261iOg¡ 0 .5.1? t z 6.9 co 301 Ã2, o. -1 65 o | 6 ¡9 6 I 6o9 AU 6 5gR OrO202q 0 rt12 I 0 6o9 cv a a t a ÞH 6ô 1g^ r)olAt?2 0.6tlt t F.9 'l C¡ C co 210 457 o.ô5952 0¡?4ôA 6.t AU a a t a 6¡l cY c1 26'l o.¿ ì22J 0 ç 600 I 6¡l Pt{ r10 312 Qr3 ,rl3? 0 6 tttS ñ.t co 234 371 0¡6 307t 0 I 1? ß 6 6¡7 Alt 66 1?2 Or1 153r o 3 ¿6¡ r 12 65 0 61 6? ß.7 CU 300 ta6 o.6 .|I 6.? Ft r{ 1c1 35t 0.5 L2-r5 o 9A15 6¡6 co 25â 6aF 0¡ô 0c o0 o ß õ14 2 6¡6 ALl 2S 595 0r0 43Ê2 0 2- 1041 t¡E cr' t.6 2ì? Or5 \7 r3 o t 0313 6o5 Rrl 2l^ 635 0.ô 3"i0 o t 2.1 0 .t 6.5 co 95 {lt Q¡2 2'r 2'r o I 9ñ I3 6r5 Art 3r 3ß3 0oO E36ß 0 3 110 ¡ 6r5 cY a2 129 Or1 ôi ôß o ô .9 0 5 6¡5 ÞF a a a o 6.4 co 312 fr5 0.6 ?".1 9 0. ¡ 6tl0 6¡4 Al' 'r+ 353 o.2 09 63 oo4rlFi 6¡4 CU _1 33 á54 0.6 0lor 0.1rttt â 6rô ¡l r't Lrt rct 0.6 of¡ at tt. t 92 6 o 6¡! e1 tq 2 1rl û.3 ß0 ?t O¡64Ò28 6ol AU 2 t10 0¡0 06 ôr o.oi0ôt 6.3 CY 10? 291 0ol 63 20 O ¡a 165'l 6¡3 Rt{ 10ô 26t 0r{ 02 9ç O¡6 itt6 ñr1 co 2ò4 I23 0.4 f5c6 o.?ô12O ll .t A r.^l 2 t2J. O¡l! 0ß?l 0¡07q02 6¡1 cu .3 ô5t O.t t162 o¡Ô402¡ 601 ePl Ê!t 2ô6 Oo2 t126 0o51145 Paqe 300 Ànova table (Variate, T) Source of d-f- M.S variation PIants 72 .06362 Treatments 3 .60797xx* Residual 30 .01s02 2 1982 Original data - abbreviations as for 1. except: Treatments intermittent pollinator exposure and bagging (AU); autogamy (AB) * missing value due either to branch death or N ( 20 PLINT f NE¡ THET{ Y t\l P EO PÀ¡ 1 Y1 co z3 a5 0¡2?0c9 0.5¿706 Y1 AIJ t t a a Y1 A8 t a ) t Y1 CU 1 35 0o02¡57 0otEtltC Y1 R l.l a a t t Y2 eo 196 923 0 t 2L4 q2 0 ¡4^156 YA ÂU 2 35 0 olrL4 0 .2.4t3ô Y2 Ac o 24 o 0o000 o ¡00OvO r2 clr 0 tO 0 o0000 o ¡ 0 00 Q O Y2 RH 1? 269 o 0 63 20 0 .?-54 ,t 61 0 ?- o61ã o .47?,0" Y3 co ., 29' Y3 Alt 3t 0 2-24ÀL o ¡ 5 gc 1ô Y3 . AB 1 4t o 0 ¿o r3 o ¡tôA dÒ Y3 CU 19 160 0 L26 6a o r 3 Ê1 ,lt Y3 RH 5 95 0 OF2OE (ì o 210 25 Y4 ' co 330 5ô9 0 å502" o ¡ 145 ô2- VI Ât' t . a t Y¡ AF 5 L'^t 0.0 ¿2 tò 0¡2 0 i ¿3 v4 c'{ 'r'l zoa o. 3 tt ff I 0.6 95I ô Yh PM t5 ?43 0.34979 Oo6 3¿å a Y' co . 60 r2a Oo472L4 O¡ 7 ã"6 3 Y5 Art 11 39 0.aå205 0.5 {9ô I Y' AB _10 ôft Or20â31 0¡4 739 ¡ vq CY 6 40 o.1ç001 1.1 9 tt0 Y5 e¡{ a I rl I q7 0 6 339 r Y6 co 20 0¡3501ô r .a Y6 Át, a a a Y6 lA a r¡ ¡ a Y6 CU o 22 o¡00000 o.00000 Y6 ÞH 11 37 0.29730 0 . 5 ?5 6 I Y7 eo 39 3?Ù 0.09459 oo3le53 Y'' AU o .67 0.00000 ô.o0000 Y'l AB o 116 g¡Og0O0 O¡oÛ2oO YI Ctd 1 61 o¡o163!l o.t2c39 a Y'l Fl ¡l tl t a Page 301 YT co 15! 954 O¡15ô2ò OrÔ091.r Yô Att 1 4'l 0.0?12ô 0r 14ñ39 Yô ¡q 6 ?l 0¡9iÔ5L O.¿9Á¡ß YC crd I ô9 0010112 4.-1 2ì52 YT PH -4 113 '0 . o 35 4C 0.tRq?." Y9 co 151 616 Ot244i4 0¡517C3 Y9 AU 129 2'19 0¡46237 0 .'l 4-l'' 3 V9 AB 22 19e it ¡ 1, t5 ?9 t).3ô721 YO cu a t a a Y9 qH ?0 39 0 0¡1?q49 0.437r'8 Y10 co 51 231 o.2zo7ô 0.4â915 Y10 Atl t 10ô 0.00926 0. ô 9Ê 3 " Y10 A8 0 103 0¡000G0 0.oooo0 Y10 cv t 3S O¡02564 0.160 t ¿ Y10 F¡H I 65 0.135 3 6 0.37t23 O.292à t Yt2 co I 108 0¡06333 q Yt2 Att 2 62 a.o 32-26 O o t ôO 9 Y12 AF t2 ,6 0o2'tô?9 o.artzt Yt2 cu 1¿ 5.1 0.2?-6 ttz u.4î5Ft YL2 Þtl 6 22 o.?-l?'r3 o.5À9¿t Y13 cn 370 673 0 r B 49 ?8 o. s352 6 Yt3 Atl 110 2't4 o.40i46 o.ñôñ21 Y13 AB 9 23 3 0¡03t¡? ù¡!'9f l1 Yt3 CY 47 93 o.505.3^ O.?q0?t Y13 ÞÉ 542 1119 0.4 ^4 36 ùrt6975 YII crl 94 264 oo15606 0.6 3q 3I Y1ô ålt 19 4C O.l. ?5 00 O.?6039 Y1+ AR 0 a? nrì0Doo tl.001ir0 Yt4 cv 70 4 0?- 0 r 17ô:I 3 o.4-?0(6 Y1A RH 6 6t 0.0 Â12ô 0. 1016 C Y15 co 11 120 0r0t16t 0.30?59 Y1ñ Ar' ¡ I a a v15 AB a a a a Y15 ev o 34 0¡O0000 O¡0000o a v15 R ¡,I a a a Anova table (Variate, T) Source of d-f. M.S variation PIants 13 .1s190 Treatments 4 .25995x** Residual 40 .02779 ÀPPENDIX 4 I{N.¡USCRIPT OF REID (1985) The paper reproduced in the following pages is ¡n press in Ford and Paton (1985), and L¡as accepted for publication in JuIy 1983. Reid, N., (1986) Pollination and seed dispersal of mistletoes (loranthaceae) by birds in southern Australia. In Ford, H.A., and Paton, D.C., (eds), The Dynamic Partnership: Birds and Plants in Southern Australia, D.J. Woolman, Government Printer, South Australia, pp. 64-84. NOTE: This publication is included on pages 303-346 in the print copy of the thesis held in the University of Adelaide Library. BEFERENCEg ÀDDICOTT, F.T . t978. Àbscission strategies in the behaviour of tropical trees. pp 381 -398. In "Tropical Trees as Living Systems". Eds, P.B. Tomlinson &M .H. Zimmerman. Cambridge U. Press, Cambridge. ALI, S.À. 1931. 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"Resource Partitioning and the Role of Competition in Structuring Lichenogtomgg Honeyeater (and Mano¡ina melgnophryg) Communities in Souther" ViËtoriã . Unpu¡Iished Ph.D. Thesis. Department of Zoology, Honash U. 7,IS[¡ILER, V. & D.S. FÀRNER. 7972. Digestion and the digestive system. pp 343-430. In "Àvian Biology. volume 2", Eds, D.S. Farner & J.R. King. Àcademic Press, Nevl York. PLÀTE 1 Principal vegetation formations in the Middleback area. Upper. Chenopod low open-shrubland dominated by saltbush in the foregrround and by bluebush and saltbush on higher grround in the distance. The dark clump Ín the centre foreground is Lycium australe, and the scattered trees and groves in the distance are Uyoporun glglvcarpum and western myall, respectively. Hiddle. I{estern myall low open-woodland in the study area, Overland paddock. The bush cover is mainly bluebush. Lower. Black oak low woodland in the study area on the boundary of Overland and Railway paddocks. The tree on the left is a western myall. Bluebush and Rhaqodia ulicina dominate the bush stratum. { PLATE 2 Upper. External appearance of the haustorium of an individual Àrnyema çIuendeng on the limb of a western myall. Note the successive reduction in haustorial branch girth from the right to the teft of the picture, indicating the vegetative spread of the haustorium doçrn the host branch. Lower. A large individual of Lvsiang exocerpi (dark central portion of the canopy) parasitising a Heterodençkum gleaefollgg. The staff is 2 m hish. \ t,**ç *6]* / PLÀTE-3 Upper. Male phase flowers of Amveme ![Janda!!g, shortly after anthesis. Note the presentation of pale pollen in the distal anthers. Two mature buds can be seen to the rÍght of the inflorescence, and four flowers which have lost all their petals are immediately in front of the inflorescence. Q t.2) Lower. Immature and ripe fruits of Amvema ggandanq. The three swollen fruits are ripe: the central one Ís grreen-ripe, and the other two are yellow-ripe. Note the basal epicarp half in the lower left of the picture. Q 7.2) PtÀrE 4 Sguashed preparations of styles and stigrmas of ÀSygma quandang in 0.1% aniline blue solution in 0.1% Na*lPOr. Fluorescence was obtained with a mercury-vapour lamp (HBO 200) and incident illuminator eguipped with a blue exciter filter and barrier filter adjusted to exclude Iight below 490 nm. Upper. The stigma and distal style of a Chinese Lantern phase bud, showing the compact appearance of the stigmatic papillae. The photograph was taken at magnification, x 100. MÍddle. The stigma and distal style of a 2-10 d old flower, penetrated by ten or more brightly fluorescing pollen tubes after (Iong) cross-pollination. Note the less compact a:rangement of the stigmatic papillae and the brightly fluorescing vascular burdles in the style. culminating at the base of the stigma. Magnification, x 100. Lower. The tip of an embryo sac in the style of a 2-10 d old flower. / I I I t I lr ) I -t ¿ t PLÀTE 5 Arrangement of the stigmatic papillae in squashed preparations of Àsvema quandang flowers of different age. Upper. Stigma of. a t-2 d old flower after (long) cross-pollination. Note the lack of adherent pollen grraÍns and the compact arangement of the stigrmatic papillae. The photograph was taken at magmification, x 250. Lower. Stigma of a 2-10 d old flower after (short) cross-pollination. Numerous germinated and fluorescing pollen grains are wedged in the clefts between the expanded stigmatic papillae. Pollen tubes can be seen penetrating between the papillae in the centre and upper right of the photograph. MagnifÍcation, x 250. I 'â I PLÀTE_É Seedlings of Àmveme qgandg$I on western myall stems. Upper left. Àn 11 mo old seedling in the hoLdfast phase, deployed on a host branch of diameter 6 mm. The persistent remains of the withered seed are attached to the hypocotyl. Incipient swelling of the host stem around the holdfast is barely noticeable. upper right. À 2 mo old seedling in the free-living phase, deployed on a 13 mm r.¡estern myall branch. After deployment in late l,larch 1983, the hypocotyl gnew beyond the host branch and died. Lower left. An 18.5 mo old seedling on a 4 mm branch of western myall. The holdfast is attached to the underside of the host stem and localised swelling of the host stem is evident around Ít. The persistent seed remains have been lifted off the host stem by the gro$rth of the hypocotyl. The endophytic system has penetrated the opposite side of the stem and produced a foliose shoot. Lower right. The same seedJ.ing aL 27.5 mo of age, with two foliose shoots growing from the shoot apex in addÍtion to the shoot from the endophytic system. -