Explosive flowering, nectar production, breeding systems, and pollinators of New Zealand mistletoes...

New Zealand Journal of Botany, 1997, Vol. 35: 345-3600028-825X/97/3503-0345 $7.00 © The Royal Society of New Zealand 1997

345

Explosive flowering, nectar production, breeding systems, andpollinators of New Zealand mistletoes (Loranthaceae)

JENNY J. LADLEY

DAVE KELLY*Department of Plant and Microbial SciencesUniversity of CanterburyPrivate Bag 4800Christchurch, New Zealand

ALASTAIR W. ROBERTSONDepartment of EcologyMassey UniversityPrivate Bag 11222Palmerston North, New Zealand

*Author for correspondence

Abstract The six New Zealand loranthaceous mis-tletoes fall into two groups based on pollination bi-ology. Four (Alepis flavida, Peraxilla colensoi, P.tetrapetala, and Trilepidea adamsii) are bird polli-nated with hermaphrodite flowers while the othertwo (Ileostylus micranthus and Tupeia antarctica)are dioecious or sub-dioecious and insect pollinated.We provide data on the pollination biology of thefive extant species (Trilepidea is extinct).

The two Peraxilla species and Trilepidea haverecently been shown to have explosive flowers. Herewe show that Alepis has weakly facultatively explo-sive flowers. The world distribution of explosivemistletoe flowers suggests that the syndrome hasarisen a number of times independently within thefamily, and is found in about half the putativelyancestral genera.

The principal avian visitors to the bird-pollinatedspecies were tui and bellbirds; introduced species arenumerically unimportant as pollinators. The nectarproduction schedules of Alepis and Peraxilla encour-age single-visit pollination as little nectar is producedafter the flowers open. However, when bird densi-ties are high, buds of Peraxilla may be forced openprematurely, encouraging multiple visits.

B96066Received 31 October 1996; accepted 9 April 1997

Alepis is highly self-compatible and its flowersachieve good seed set in the field even when allpollinators are excluded by mesh bags, partly be-cause pollen contacts the already-receptive stigmabefore the bud opens. Unvisited Peraxilla buds donot open, but their morphology allows a low level(11-22%) of self-pollination in the bud.

The sex ratio of Tupeia at Wainui (Banks Penin-sula) was 3:1 female:male, while Ileostylus atWakefield (Nelson) was subdioecious with a 2.5:1:1female:male:hermaphrodite ratio. HermaphroditeIleostylus plants set seed even when pollinators areexcluded, so self-pollination is possible in this spe-cies.

Results suggest different species vary in theirsusceptibility to pollen limitation affecting reproduc-tion. The insect-pollinated species have unspecial-ised pollination syndromes and are probablyadequately pollinated by native and/or introducedinsects; Ileostylus is also self-compatible. The bird-pollinated species are more susceptible with special-ised pollination systems depending principally onendemic birds, but the effect is reduced in Alepis asits flowers can open themselves and it achieves goodseed set even when pollinators are excluded.Peraxilla spp. seem most at risk with obligately-explosive flowers and only low seed set withoutpollinators. Historical declines in the North Islandhave been greatest in the species with the most ex-acting pollination requirements. Long-term conser-vation of these mistletoes will require conservationof tui and/or bellbirds.

Keywords Loranthaceae; Peraxilla; Alepis;Tupeia; Ileostylus; Trilepidea; bird pollination; self-compatibility; dioecy; breeding systems; explosiveflowering; nectar production

INTRODUCTION

New Zealand has six species of native loranthaceousmistletoe, and there is concern that all have declinedin abundance (de Lange et al. 1997). Originally this

346 New Zealand Journal of Botany, 1997, Vol. 35

was attributed to habitat clearance, overcollecting bybotanists, and introduced brushtail possums(Trichosurus vulpecula), which all may increasemortality in adult mistletoes (Norton 1991). RecentlyLadley & Kelly (1995a, 1995b, 1996) suggested thatreproductive difficulties in pollination and dispersalcould have affected recruitment and been partiallyresponsible for the declines. In this paper we providedata on pollination of extant native Loranthaceae andevaluate whether they are at risk from pollinationfailure.

Within the 78 genera of Loranthaceae worldwide(Barlow et al. 1989), most species have large bird-pollinated hermaphroditic flowers, in one of twobasic forms: those that open suddenly when visitedby a pollinator, known as explosive flowers; andthose that open normally over a longer period andare then visited by birds. Explosive flowers may beobligate, where the flower cannot open itself unlessvisited by a bird, for example as in mostLoranthaceae (Docters van Leeuwen 1954; Feehan1985; Polhill 1989; Ladley & Kelly 1995a); or fac-ultative, where a flower has a period when it is readyto be sprung but will eventually open even if notvisited, for example as in the mangrove Brugierahainesii (Noske 1993). Explosive flowering was firstdescribed by Evans (1895) for two African mistle-toes, Tapinanthus kraussianus and Erianthemumdregrei. In such flowers, anthers characteristicallydehisce in the mature bud, and mature buds usuallycontain large amounts of nectar (Docters vanLeeuwen 1954).

Explosive mistletoe flower mechanisms are eithertwo-stage (flower opening and pollination take placein separate movements) or the more specialised one-stage (a single movement achieves both; Pohill1989). In both cases some degree of behaviouralspecialisation by the pollinator is required. If onlycertain birds know how to, or are large enough to,open flowers then the range of potential pollinatorsfor the plants is reduced. For example, in Indonesia,explosive Macrosolen flowers offered to four spe-cies of nectarivorous birds which had no previousexperience with the plant were not opened (Doctersvan Leewen 1954, p. 139). Moreover, if the plantspecies becomes uncommon, previously capablepollinating bird species may forget how to open theflowers (Ladley & Kelly 1995a).

The composition of the pollinator assemblageamong birds which visit explosive mistletoe flow-ers is also affected by dominance relationships be-tween the birds, which in turn is modified by theexact timing of nectar production. In most species,

the buds already contain nectar so that they providea tamper-proof container with an assured reward(Ladley & Kelly 1995a). Therefore, foraging on ripeunopened buds is likely to be energetically morerewarding than revisiting already-opened flowers. InAfrica, Gill & Wolf (1975) showed that largersunbirds tend to feed principally on unopened buds,excluding the smaller bird species which thereforehave to concentrate on already-opened flowers.

Although most Loranthaceae are bird-pollinated,some species have insect-pollinated flowers and aredioecious (having separate male and female plants);the flowers of these species are usually small and notbrightly coloured (Kuijt 1969). New Zealand has sixnative Loranthaceae. Four, Alepisflavida*, Peraxillacolensoi, P. tetrapetala, and Trilepidea adamsii arebird-pollinated with hermaphroditic flowers. Theremaining two species, Ileostylus micranthus andTupeia antarctica, are thought to be insect-pollinated(Barlow 1966) and are dioecious or sub-dioecious.All species are endemic, except for Ileostylus whichalso occurs on Norfolk Island. Trilepidea has be-come extinct this century (Norton 1991) but the otherspecies are still extant.

Recent research into the floral biology of the NewZealand Loranthaceae has documented explosiveflower opening in Peraxilla and Trilepidea (Ladley& Kelly 1995a, 1995b; Kelly etal. 1996). Explosiveflowers in Loranthaceae are well known from Af-rica and to a lesser extent India and Indonesia, butwere previously unreported from Australasia. There-fore, the pollination systems of Peraxilla andTrilepidea are most similar to those of the Africanmistletoes. However, other data suggest that the twogroups are not closely allied within the family. Allof the New Zealand Loranthaceae are thought to beancestral relict genera, based on chromosome num-bers and the presence of ancestral characteristics,including secondary runners (Kuijt 1969; Barlow1983; Martin 1983). Therefore, either explosiveflowers have arisen independently several times, orthe current view of New Zealand Loranthaceae asancestral must be revised.

Previous research on the floral biology and pol-lination of the New Zealand mistletoes is limited.Smart (1952) showed that Tupeia antarctica isdioecious. The four-petalled green-yellow flowers of

*Plant nomenclature follows Allan 1961, Connor &Edgar 1987, and Webb et al. 1988.

Ladley et al.—Mistletoe pollination 347

both sexes are very small and apparently pollinatedby insects, such as small flies, which are attractedby the honey disc in the centre of the flower.Ileostylus micranthus is thought to have asubdioecious breeding system (i.e., there are somehermaphrodite individuals), and the flowers are in-sect-pollinated (Menzies 1947). Ileostylusmicranthus is apparently the only subdioecious spe-cies in the Loranthaceae. More recently Ladley &Kelly (1995a, 1995b) and Kelly et al. (1996) de-scribed explosive pollination in Peraxilla andTrilepidea, and reported that Peraxilla spp. are self-compatible. In Peraxilla, self-pollination was pre-sumed to occur when the petals abscise, lifting theattached anthers over the stigma which remains at-tached to the ovary (Ladley & Kelly 1995a). Al-though Peraxilla flowers are principally adapted forbird pollination, the flowers of P. tetrapetala are alsosometimes opened by native Hylaeus bees (Kelly etal. 1996). There is no other published work on NewZealand mistletoe floral biology. Outbreeding isthought to be the norm within the family generally,although self compatibility may be common(Bernhardt & Calder 1981; Barlow 1983). Standardthroughout the Loranthaceae is the production ofonly one seed per fruit in a pseudoberry (Kuijt 1969).

The general aim of this study was to provide amore complete understanding of the floral biologyof the surviving New Zealand Loranthaceae. In par-ticular, six areas were addressed where informationin the literature is inadequate. For bird-pollinatedspecies (Alepis flavida, Peraxilla colensoi, and P.tetrapetala): (1) what are the main avian pollinatorspecies, and how is pollination effected? (2) Whenis nectar produced, and how does this affect visita-tion? (3) Is Alepis self-compatible? For insect-pol-linated species (Ileostylus micranthus and Tupeiaantarctica): (4) what are the sex ratios of thesedioecious species in the field? (5) Is Ileostylus self-compatible? And for all species: (6) are pollinationdifficulties likely to be limiting reproduction in anyof the New Zealand Loranthaceae?

METHODS AND MATERIALS

Study sites and speciesAll five extant Loranthaceae of New Zealand wereincluded in the study. P. colensoi was studied atWakefield (grid reference NZMS 260 N27 121802,41 °23'S 173°02'E), at the boundary of Motueka andMoutere Ecological Districts, 30 km south-west ofNelson. The average annual rainfall in the area is

approximately 1100 mm. P. colensoi plants weresituated in isolated Nothofagus menziesii stands sur-rounded by pasture along the length of Pigeon Val-ley (60 to 120 m a.s.l.). /. micranthus was studied atWakefield growing in a large stand of Podocarpustotara (60 m a.s.l.), and at Otanerito (N37 145074,43°51'S 173°04'E), Akaroa Ecological District,Banks Peninsula, growing on shrubs of Coprosmarotundifolia and Melicope simplex in open kanuka(Kunzea ericoides) forest at an altitude of 50 m. T.antarctica was studied at Wainui (N37 024089,43°50'S 172°55'E), also in the Akaroa EcologicalDistrict. The site is 10 m a.s.l. and it has an averageannual rainfall of 700 mm. A large population ofTupeia grows on the introduced shrubChamaecytisus palmensis along a 500 m strip ofroadside. Two species (A. flavida and/3, tetrapetala)were studied growing on Nothofagus solandri var.cliffortioides hosts at Craigieburn (K34 050831,43°09'S 171°43'E), Craigieburn Ecological District,Canterbury. The site is in intact native forest domi-nated by N. solandri var cliffortioides at Jacks Passat 940 m altitude in the Craigieburn Range and hasan average annual rainfall of 2000 mm. For moreinformation on the sites see Ladley & Kelly (1996).

Pollination observations of P. tetrapetala weremade at four additional locations: Belgrove(N28 061724,41°28'S 172°57'E), 10 km south-westof Wakefield; Lake Ohau (H38 557619, 44°12'S169°49'E); Waiouru (T20 559908, 39°27'S175°52'E ); and Little Barrier Island (S08 972536,36°12'S 175°02'E). At Belgrove, Lake Ohau, andWaiouru the mistletoes were growing on N. solandritrees surrounded by open grassland. On Little Bar-rier the P. tetrapetala was growing near the top ofthe island (700 m a.s.l.) on Quintinia serrata.

Bird-pollinated species

Observations on flower visitors and pollinators werecarried out for A. flavida, P. colensoi, and P.tetrapetala. In 1992/93, observations were made inthe field of birds visiting flowers; in later years,videotapes were made of flowering plants and vis-its per hour were noted from the tapes. Native beesalso open flowers of P. tetrapetala, and visit flow-ers of P. colensoi, but produce lower fruit set rates(Kelly et al. 1996); the effectiveness of insects aspollinators on the bird-adapted mistletoes will beconsidered further elsewhere.

Nectar production was measured in summer1992/93 {Alepis, P. colensoi, and P. tetrapetala) and1993/94 (P. colensoi only) by enclosing buds in fine-mesh cotton bags to prevent nectar being harvested.


From the day that flowers self-opened (in Alepis) orripened enough to be opened by hand (in Peraxilla),the nectar production per flower was measured dailyusing micropipettes (5 |al to 100 ul) and then the bagswere replaced on the flowers. The sugar content ofthe nectar was measured in brix (% w/w: weight ofsugar per weight of solution) with a hand-held Atagorefractometer, and the results converted to % w/volsolution (so that sucrose equivalents per flower couldbe evaluated; Kearns & Inouye 1993). In 1995/96,we measured Peraxilla nectar production again, thistime taking careful note of the degree of flower ripe-ness. Measurements were made of: (I) prematurebuds that were not quite ripe but were able to beforced open using more pressure than normally re-quired for 'ripe' flowers; (2) ripe buds — showingcoloration of ripe buds and easily opened by hand;and (3) overripe buds that were older and had be-gun to show signs of aging such as small splits inthe corolla. Once again, the volume was measuredwith capillary tubes and the sugar content with a re-fractometer.

Pollination experiments to test for self-compat-ibility, cross-pollination, and autogamy were carriedout on randomly selected reproductive A. flavidaplants at Craigieburn (seven in 1992/93 and five in1996/97). In 1992/93, inflorescences on each of theseplants were tagged and randomly allocated to one offour experimental treatments: bagged and self-pol-linated by hand; bagged and cross-pollinated by handusing pollen from several nearby plants; bagged andnot hand-pollinated; and unbagged control. The bagsused were made of fine cotton mesh buttercloth. Thesame procedure was used in 1996/97 except that thehand-self-pollination treatment was replaced withenclosing buds in a wire mesh cage which excludedbirds but not insects. Fruit set on the individual flow-ers on each inflorescence was monitored every 2—3weeks until fruit ripened. The data were analysed inS-plus statistical software using a generalised linearmodel with binomial error distribution and logit linkfunction. Self-compatibility has already been docu-mented in both Peraxilla species (Ladley & Kelly1995a; Kelly et al. 1996).

Self-compatibility was also assessed in Alepis byexamining harvested styles from buds and openflowers for pollen tube growth. The styles were pre-served in formalin acetic acid fixative (FAA) andthen cleared in 4N NaOH for at least an hour at 60°C,rinsed in distilled water for > 2 hours, and thenplaced in decolourised aniline blue stain mixture(K2PO4 with 0.0015% aniline blue) for at least 20hours. The styles were then mounted in a drop of

aniline blue mixture and viewed under a UV fluo-rescence microscope (Snow & Spira 1991).

The morphology of buds of A. flavida, P.colensoi, and P. tetrapetala was described in the labusing FAA-preserved material. The relative posi-tions of the stigma and anthers inside a number ofmature buds and flowers were noted to investigatethe possibility of self-pollination prior to the budopening (autogamy). For both Peraxilla species, wemeasured on fresh material the area of the stigma thatappeared to be receptive using the simple presence-of-bubbles version of the peroxidase test (Zeisler1938). The position and the proportion of the areathat was receptive was scored, after 60 seconds in3% hydrogen peroxidase, for five buds of each of thethree bud stages recognised above (premature, ripe,over-ripe) from four trees for both species. For analy-sis, the proportions were arcsine-square-root trans-formed; analysis of variance was carried out usingtype III sums of squares treating plants and treat-ments as fixed effects; comparison of means per-formed using Tukeys HSD difference tests (P <0.05); and the means back-transformed for presen-tation.

Insect-pollinated speciesSex ratios for the /. micranthus and T. antarcticapopulations were measured by a census of taggedreproductive plants at Wakefield and Wainui, respec-tively, during the flowering season. Plants of T.antarctica were classified as either male or femaleand /. micranthus plants as either male, female, orhermaphrodite, based on their flower morphology.

The possibility of self-pollination within asubdioecious population of/, micranthus was inves-tigated by tagging five pairs of branches on fiveplants (four hermaphrodite and a female) at Otaneritoin October 1995. Within each pair of branches, onebranch was bagged in fine nylon mesh to excludepotential insect pollinators. The other branch was leftopen as a control. The number of flower buds wascounted just before flowering commenced. The bagswere removed once all anthers had been shed, andthe number of ripening fruits was counted in Janu-ary 1996.

RESULTS

The overall timing of flowering and flower charac-teristics of the New Zealand Loranthaceae are givenin Table 1. The bird-pollinated species flowered in


mid summer, while the insect-pollinated speciesflowered in spring.

Visitors to bird-pollinated speciesObservation on bird species visiting Peraxilla flow-ers showed that tui {Prosthemaderanovaeseelandiae) and bellbirds (Anthornismelanura) were by far the most numerous avianflower visitors (Table 2). A few individuals of otherbird species were seen in mistletoes but some mayhave been searching for invertebrates. Only at onesite have we seen birds other than tui and bellbirdsdefinitely opening Peraxilla buds: at Lake Ohau in1996/97 silvereyes (Zosterops lateralis) andchaffinches (Fringillacoelebs)opened/*, tetrapetalabuds.

Bellbirds were present at all sites, whereas tui

were absent from Craigieburn and Lake Ohau. AtCraigieburn all P. tetrapetala bird-pollination wasattributed to bellbirds. When both were present, tuiwere more common than bellbirds on both Peraxillaspecies in Nelson, but bellbirds were more commonat Waiouru and Little Barrier. At Wakefield andBelgrove, tui were dominant and aggressive (to othertui, to bellbirds, and to any other species which vis-ited the flowering Peraxilla plants) chasing awayeven nesting house sparrows (Passer domesticus).Presumably the relative abundance of the varioushoneyeaters is determined by their local densities,the attractiveness of alternative food sources at eachsite, and competitive relationships between the birdspecies.

Alepis were observed only at Craigieburn (wheretui are absent). Flowers were visited by bellbirds and,

Table 1 Flower characteristics of the extant New Zealand Loranthaceae. All data are from the sites andyears covered in this paper except where noted. Means are ± 95% C.I.

Species Flowering season Flower colour Petal length (mm) Pollinator Flower morphology

Peraxilla colensoiP. tetrapetalaAlepis flavidafleostylus micranthusTupeia antarctica

Mid Dec-JanDec or JanMid Jan—FebMid Oct-NovMid Aug—Oct

RedRed3

YellowGreenish-yellowGreen

42.226.616.22.5 b

1-2

±0±1±0

c

.7

.0

.8

birdbirdbirdinsectinsect

hermaphroditehermaphroditehermaphroditesub-dioeciousdioecious

a, yellow on Little Barrier Island; b, Menzies (1947); c, Smart (1952).

Table 2 Bird species observed visiting flowering Peraxilla and Alepis plants. Bellbirds were present at all sites buttui only at some, as indicated.

Mistletoespecies

P. colensoiP. colensoiP. colensoiTotalP. tetrapetalaP. tetrapetalaP. tetrapetalaP. tetrapetalaP. tetrapetalaP. tetrapetalaP. tetrapetalaP. tetrapetalaTotal

A. flavida

Site

WakefieldWakefieldWakefield

BelgroveBelgroveLittle BarrierWaiouruCraigieburnCraigieburnCraigieburnLake Ohau

Craigieburn

Tuipresent?

yesyesyes

yesyes

Island yesyesnononono

no

Total hours ofYear i

1994/951995/961996/97

1993/941995/961995/961994/951994/951995/961996/971996/97

1996/97

Dbservation

32.928.2

9.270.3

2.82.09.22.4

24.233.712.235.4

121.9

14.4

Bird species(total number of visits)

Tui (39), bellbird(l)Tui (4), bellbird (2), silvereye* (2)Tui (6)Tui 49, bellbird 3, silvereye* 2Tui (17)Tui (3), house sparrow* (1)Bellbird (5), tui (1)Bellbird (2)Bellbird (17)Bellbird (14)Bellbird (4)Bellbird (5), chaffinch (5), silvereye (Of),Tui 21, bellbird 47, chaffinch 5, silvereye Of,house sparrow* 1Bellbird (1), silvereye (1)

* These birds were not confirmed to be pollinating flowers and may have been foraging for insects or not feeding.tSilvereyes were seen opening P. tetrapetala flowers at Lake Ohau but did not appear on the 29 hrs of videotape.


o

CDQ_CD

_=!O

oCD

P.colensoi P.tetrapetala

Fig. 1 Nectar production (|j.l) in Peraxilla spp. flowerswith increasing age after opening. Data are for 1995/96except where noted. In 1992/93, Peraxilla flowers wereopened by hand when the buds ripened, and bagged be-tween measurements to prevent nectar harvesting. In 1995/96, flowers were classified into three stages of ripeness(see text for details) prior to sampling. For sample sizessee Table 3.

less frequently, by silvereyes; the low visitation ratesper hour in Table 2 are an artifact of the small sizeof the videotaped Alepis plants. All of the observedforaging visits were to newly opened flowers. Theflowers of Alepis were classified as non-explosiveby Ladley & Kelly (1995a) since bagged flowers doopen unaided (i.e., are not obligately explosive, incontrast to Peraxilla). However, Godley (1979, p.445) saw native bees (Hylaeus agilis: Hymenoptera,Colletidae) successfully opening buds, and Ladley& Kelly (1995a) reported seeing a bellbird tryingunsuccessfully to twist open unripe buds. We havenot observed any Alepis buds being opened by birdsor bees despite careful searching, including at siteswhere Hylaeus agilis was opening flowers of P.tetrapetala (Kelly et al. 1996). Therefore, Alepisflowers seem to be weakly facultatively explosive,and are sometimes opened by native bees and per-haps also by bellbirds, but this is far less commonthan for Peraxilla.

For the two Peraxilla species virtually all theforaging bouts were on mature unopened buds. Laterin the season when most Peraxilla flowers were al-ready opened, it was difficult to see whether a birdwas probing an open flower or twisting a ripe bud.Some flowers were probably revisited after beingopened, but overall there was a clear emphasis onvisiting buds rather than open flowers in Peraxilla.After flowers are opened, there are colour changesover the next 24—36 hours in both Peraxilla (fromyellowish-red to dark red) and in Alepis (from yel-low to orange) which would allow birds to distin-guish newly-opened from older flowers.

Table 3 Nectar energy production of Peraxilla species measured as sucrose equivalents(mg/flr). In 1992/93, flowers were opened by hand when the buds ripened, and baggedbetween measurements to prevent nectar harvesting. In 1995/96, flowers were also classifiedinto three stages of ripeness (see text for details) prior to opening. The subsequent productionof P. tetrapetala flowers was followed for a further 48 hours. Buds cease to produce nectarabout the time they become ripe (i.e., ready to be opened without excessive force).

P. colensoi

P. tetrapetala

Year

1992/31995/961995/961995/961992/931995/961995/961995/96

Stage at opening

mostly ripeprematureripeoverripemostly ripeprematureripeoverripe

n

12820892148203612

Day 1

9.622.475.155.804.522.474.584.01

Day 2

————2.280.060.02

Day 3

----0.220.000.00

Total

5.80*

4.984.644.02

(±se)

——

+ 0.73-

+ 0.34±0.27+ 0.34

* Assuming negligible production of nectar in overripe flowers after they are opened.


Nectar production in bird-pollinated speciesIn total, all three bird-pollinated species producedlarge quantities of nectar and sugar (Tables 3 and 4),especially the two Peraxilla species. In otherLoranthaceae worldwide only the AustralianMuellerina eucalyptoides had greater energy produc-tion per flower (Table 4).

For the New Zealand species there was usuallyvery little nectar produced after the flower openeditself (Alepis) or ripened enough to be opened by ananimal {Peraxilla). Indeed, for A. flavida in 1992/93 there was zero nectar production after the first dayin all of the 15 flowers measured. In 1992/93, P.tetrapetala flowers also produced negligible nectarvolume after opening (Fig. 1), with only 1.5% of thetotal produced after day 1. For/3, colensoi in 1993/94,72.1 % of all nectar volume was presented whenthe flowers were first opened, and some (26.6%) wasproduced during the following day. The productionafter opening could be because either some of theflowers genuinely continued producing nectar afterripening (18% had their peak nectar production a dayafter opening) or they had been forced open prema-turely by hand a day before they were really ripe. Avery small amount of nectar (1.3% of the total) wasproduced on days 3 and 4. Converting these volumesto sucrose equivalents showed that in the summer of

1992/1993, P. colensoi flowers produced twice asmuch sugar (9.62 mg) as P. tetrapetala (Table 3).

In the summer of 1995/96, we further tested thepossibility of anticipating peak production by pre-maturely opening flowers of Peraxilla. Flowers thatwere not quite ripe (premature) contained only halfas much nectar volume (Fig. 1) and sugar (Table 3)as fully ripe flowers. In P. tetrapetala, these prema-turely opened flowers went on to produce more nec-tar over the next 48 hours so that in the end they hadproduced about the same total as the flowers thatwere opened when ripe (Fig. 1). Ripe and overripeP. tetrapetala flowers essentially contained all theirnectar when opened and produced very little subse-quently. The further production of nectar in openedflowers was not studied in P. colensoi in that sum-mer, but premature buds also contained only half thenectar seen in ripe buds. If we assume that over-ripeflowers contain all the nectar that is likely to be pro-duced by a flower, the sugar content was down inthis species compared with 1992/93 (Table 3).

Bud structure, self-pollination, and self-compatibility in bird-pollinated speciesMature buds of A. flavida and the two Peraxillaspecies form fenestrae (splits between the petals) asseen in African explosive-opening mistletoes. In all

Table 4 Nectar quantities per flower for Loranthaceae. Where a range is given, the values are the highest and lowestmeans from different datasets.

Species

Muellerina eucalyptoidesPeraxilla colensoiPeraxilla tetrapetalaPhragmanthera dshallensisAmyema miqueliiLysiana exocarpiAmyema pendulaAmyema quandangAlepis flavidaAmyema miraculosaTapinanthus bangwensisGlobimetula brauniiGaiadendron poasense

Nectar in closed bud

QuantityHi

50.635.2-43.520

4.73.0

Sugar %(w/w)

14.310.712.211.617.5

8.310.4

Sucroseequivalents

(mg/bud)

5.15-9.624.01^.583.85

0.390.31

QuantityHi

69.112.635.712.93.55.1

3.74.72.411.61.30.750.65

Nectar in open flower

Sugar %(w/w)

**

17.536.5

21.424.3

*33.89.0

11.216.0

Sucroseequivalents(mg/flower)

6.345.80*4.02-4.98*0.671.98-2.150.93-1.710.85-1.261.07-1.08

0.500.070.07

References

6this paperthis paper31,64,62,62,6this paper1557

* Total production (± standard error) over life of flower (2-4 days).References: 1: Bernhardt (1984); 2: Bernhardt & Calder (1981); 3: Gill & Wolf (1979); 4: Ford (1979); 5: Kirkup(1984); 6: Reid (1986);7: Wolf et al. (1976).


Table 5 Stigma receptivity in Peraxilla species, (a)The proportion of the stigma that is receptive in buds ofthree ages, measured as the area of the stigma that producedbubbles after one minute of submergence in 3% hydrogenperoxide. Within each column, means (back-transformedfrom the arcsine-square-root transformed data) with thesame superscript are not significantly different (TukeysHSD test, P < 0.05). (b) Analyses of variance on theproportions using type III sums of squares treating plantsand treatments as fixed effects.

(a)

Stage

PrematureRipeOver-ripe

(b)Species

P. tetrapetala

P. coiensoi

Proportion of stigma receptive

P.tetrapetala

0.18a

0.36b

0.65c

Source df

stageplantstage'errorstageplantstage"error

23

'plant 65923

"plant 659

P.coiensoi

MS

0.8650.0710.1300.0450.7930.1190.1620.053

0.2P0.58b

0.71b

F

19.061.562.86

14.912.243.04

P

<0.00010.21030.0183

<0.00010.09620.0134

three species, the anthers dehisce and pollen is re-leased prior to the bud opening, and observations ofsectioned buds showed that the stigma and anthersare in close proximity at the tip of the bud. Thestigmatic surface is firmly pressed up against thetrichome cap, formed by the underside of the tips ofthe petals, and the anthers are packed tightly aroundthe style, just below the stigma.

In mature A. flavida buds, the lower half of thestigma is in direct contact with the dehisced anthers.Fluorescence microscopy showed pollen tubegrowth in styles from both open flowers (7.45 ± 2.36tubes per style, mean ± 95% CI) and from buds (5.19± 1.34 tubes), showing that pollen does get onto thestigma and germinate before the flowers open.Therefore, the stigma must be receptive before thebud opens, i.e., there is no dichogamy.

In both Peraxilla species, the first part of thestigma to ripen is the distal part (furthest from theanthers) and receptivity spreads towards the base ofthe stigma as it ripens (Table 5a). Hence self-pollenis only likely to contact a receptive surface in over-ripe buds, even though the anthers dehisce well be-fore the flower is ready to be opened. This isconfirmed by the finding that in Peraxilla buds,pollen tubes are found in the styles of only very old,over-ripe buds (Robertson, Kelly, and Ladley

Table 6 Effect of different pollination treatments on Alepis flavida plants atCraigieburn. (a) Mean fruit set (%, with number of flowers in parentheses), (b)Overall significance tests for analysis of effect of pollination treatments on fruitset, by means of generalised linear models with binomial errors and logit linkfunctions. Plants were inserted into the model first as a block effect andtreatments tested next. In both cases there was a significant plant (block) effect;treatments differed significantly only in 1996/97.

(a)Treatment Fruit set 1992/93 Fruit set 1996/97

Open controls (bird pollinated) 82.5 (610)Cross-pollinated by hand 58.3 (108)Self-pollinated by hand 48.3 (85)Bagged, pollinators excluded 64.7 (258)Caged (birds excluded, insects not) —Number of plants 7

(b)Residual

Year Model df Deviance df

71.3(754)83.2 (68)

90.2(151)89.6 (262)

5

Residualdeviance Pr (Chi)

1992/93

1996/97

NullplantstreatmentsNullplantstreatments

64

44

64.86.87

84.155.8

332723231915

99.9635.1128.24

176.592.4536.61

<0.0010.14

<0.001<0.001


unpubl. data). The only differences between thespecies in stigma receptivity are that ripe P. colensoibuds have a bigger proportion of the stigma recep-tive than in P. tetrapetala, and there is no signifi-cant subsequent increase in receptive area for P.colensoi (Table 5). There is a significant plant-stageinteraction suggesting that some plants' stigmasripen at different rates which could affect selfingrates.

A high percentage of flowers set fruit in Alepisunder all pollination treatments, including baggedflowers from which all pollinators were excluded(Table 6). Statistical analysis showed that there wasa significant plant effect in both years (P < 0.001)but a significant difference among treatments onlyin 1996/97. However, in both years there was verygood fruit set under all treatments. This confirms thepollen tube and structural information suggestingthat self-pollination occurs readily, and also showsno significant difference between flowers hand-pol-linated with self- or cross-pollen.

Insect-pollinated speciesSurveys of the sex ratios of populations of /.micranthus and T. antarctica revealed that for /.micranthus at Wakefield there was a ratio of 2.5:1:1(female:male:hermaphroditic plants), while T.antarctica had a ratio of 3:1 (female:male plants).

Results from the experiment on self compatabilityof/, micranthus showed that there was considerablevariation between plants (Table 7). Some leaves andflowers were damaged by caterpillar predation inboth bagged and control branches, especially onplants 3 and 5. One plant was structurally femalewith only rudimentary anthers and this plant set noseed inside the bag, showing that the bag did pre-vent movement of pollen. While the other plantswere all structurally hermaphrodite, one (plant 3) setno ripe fruits in either treatment. The remaining three

hermaphrodites all set some seed when pollinatorswere excluded.

DISCUSSION

Distribution of explosive floweringExplosive flowers have been reported in at least 17genera of Loranthaceae worldwide (Table 8). Barlow(1983) reviewed the evolutionary relationships of theLoranthaceae as a whole and described four majorgroups, based on chromosome numbers and pre-sumed-ancestral characters (such as root parasitismand epicortical runners). The first group containsrelict genera found in Australia, New Zealand, andSouth America (Gondwana is the putative centre oforigin of the family) with a variety of ancestral char-acteristics, all with x = 12 chromosomes. The sec-ond group are also x = 12 but include recentlydiversified groups in south-east Asia and India. Thefinal two groups are large, recently diversified col-lections of species in the New World (x = 8) and theOld World especially Africa (x = 9). These last twogroups are each more closely related to the ances-tral groups than to each other (Barlow 1983).

It is in the Old World group, centred onTapinanthus in Africa, that explosive flowers arebest known. Polhill (1989) recorded that most of the25 African genera have some explosive-floweredspecies. Tapinanthus alone consists of some 200species, and many of these have explosive flowers.However, from Table 8 it is apparent that explosiveflowers are found in all four of Barlow's majorgroups. While the more advanced x = 12 group andthe New World x = 8 group have only one recordedgenus each with explosive flowers, it is striking howmany of the putative ancestral relict genera are nowproven or suspected to have explosive flowers. Inthis group, four genera have explosive flowers, four

Table 7 Fruit set in bagged (pollinator-exclusion) and unbagged Ileostylusmicranthus flowers, Otanerito, 1995.

Plant

12345

Host

Melicope simplexCoprosma crassifoliaMelicope simplexCoprosma crassifoliaCoprosma crassifolia

% Fruit set (n)

Sex Control branch

femalehermaphroditehermaphroditehermaphroditehermaphrodite

40.4 (57)40.8(125)

0(31)no data0(31)

Bagged branch

0(48)6.4 (78)0(38)

28.8 (80)12.5 (24)

Table 8 Worldwide distribution of explosive flowers in Loranthaceae. Groups and plant names follow Barlow (1983) and Barlow et al. (1989), respectively.

Group and Mistletoe species Region Pollinating birdsa Flower typeb Floral Characteristics Referencec

Ancestral, x = 12Peraxilla colensoiPeraxilla tetrapetalaAlepis flavidaTrilepidea adamsiiTristerix tetrandusTristerix aphyllusMore advanced, x = 12Macrosolen parasiticusMacrosolen cochinchinensisAdvanced New World, x = 8Psittacanthus spp.Advanced Old World, x = 9Tapinanthus spp.

Erianthemum spp.Phragmanthera spp.

Agelanthus spp.Globimetula spp.

Moquiniella spp.Englerina spp.Taxillus cuneatus

Taxillus tomentosusTaxillus recurvusDendrophthoe falcataDendrophthoe neelgherrensis

New ZealandNew ZealandNew ZealandNew ZealandSouth AmericaSouth America

India, Sri LankaJava

honeyeatershoneyeatershoneyeaters

sunbirdsflowerpeckers

S/Cent. America hummingbirds

Africa

AfricaAfrica

AfricaAfrica

AfricaAfricaIndia, Sri Lanka

Sri LankaIndiaIndiaIndia, Sri Lanka

sunbirds, chats

sunbirdssunbirds

sunbirds

sunbirdsflowerpeckers,

sunDirussunbirds

flowerpeckerssunbirds

222122

22

2

1

11

12

212

22

Dendrophthoe suborbicularis Sri Lanka sunbirdsDendrophthoe pentandra Java sunbirdsDendrophthoe nova-guineae New Guinea

Flowers do not open unaided. Bagged flowers set some seed. 14Flowers do not open unaided. Bagged flowers set some seed. 14Flowers open unaided; bagged flowers set seed. 9, 14Extinct. Explosive opening inferred from structure of open flowers. 14Buds have fenestrae but explosive opening not confirmed. 10Buds have fenestrae but explosive opening not confirmed. 10

Bagged buds may (ref. 13) or may not (ref. 14) open and self-pollinate. 4, 11Flowers symmetrical, bagged buds do not open but do set seed. 5

Orange-red flowers unzipped upwards by short-tongued hummingbirds. 13

1 or 2 Two groups of species: 1. Buds with fenestrae, flowers 5, 6, 7,12, 15asymmetrical, one-stage pollination. 2. Buds without fenestrae, flowerssymmetrical, two-stage pollination. Some spp. have extended nectarproduction.Symmetrical orange flowers, fenestrae present in the buds, lots of nectar. 6, 7, 15Some species asymmetrical, short nectar production, others long nectar 7,8,15production.Similar pollination method to Phragmanthera. 15No fenestrae, flowers asymmetrical. Some spp. have extended nectar 7, 12, 15production.Similar pollination method to Globimetula. 15Flowers asymmetrical, petals don't split completely. 5, 7Flowers green-yellow; nectar renewed after visit; one fenestra in corolla 2, 3,4, 11tube.Flowers asymmetrical when open. 11Nectar not renewed after first visit. 4Red flowers; no self pollination in unopened buds; nectar fills corolla tube. 1, 2, 4, 5, 11Flowers slightly asymmetrical, nectar not renewed after opening, able 2, 3, 4, 5, 11to self-seed.Exploding flowers can be heard some metres away. 11

2 Flowers symmetrical, last 24 hrs, lots of nectar. Bagged buds don't set seed. 52 Has fenestrae in mature buds. 5

a As listed in source. Bird families mentioned: sunbirds = Nectariniidae, flowerpeckers = Dicaeidae, honeyeaters = Meliphagidae; hummingbirds = Trochilidae;chats = Anthreptes spp.b Types of explosive flower opening: 1 = One stage opening, 2 = Two stage opening.c References: 1 Ali (1931), 2 Ali (1932), 3 Davidar (1983), 4 Davidar (1984), 5 Docters van Leeuwen (1954), 6 Evans (1895), 7 Feehan (1985), 8 Gill & Wolf(1975), 9 Godley (1979), 10 Johow (1900), 11 Keeble (1896), 12 Kirkup (1984), 13 Kuijt (1969), 14 Ladley & Kelly (1995a, 1995b), 15 Polhill (1989).

•zNa>

3

OC

P

I

o


apparently do not (Nuytsia, Atkinsonia,Gaiadendron, and Notanthera), and one (Tupeia) isinsect-pollinated.

Interestingly there has been no demonstrated ex-plosive flower opening in any AustralianLoranthaceae (Calder et al. 1979). Armstrong (1979)stated that birds have been observed visiting un-opened mature buds of Amyema and forcing the budsopen. However, he then goes on to say that the flow-ers of Amyema are not dependent on explosive open-ing (i.e., are not obligately explosive). inA. pendula,Bernhardt & Calder (1981) considered whether thespecies is explosive but did not come to a clear con-clusion. They showed that buds will separate "withgentle probing for nectar with a capillary tube", andthey reported that a large number of buds wither withthe corolla still fused at the top. On the other hand,Bernhardt (1983, p. 89) states "no Amyema specieshad ever been described displaying the 'explodingflower' mechanism common to so many Paleo-tropical genera". However, the evidence hints thatsome Amyema spp. may be at least facultativelyexplosive, as we suggest for Alepis. Explosive flow-ering may be surprisingly cryptic, especially if fac-ultative, as recent New Zealand discoveries haveshown. The dividing line between facultatively ex-plosive flowers, and normal flowers which may beoccasionally forced open prematurely by birds, is notsharp; however, facultatively explosive flowersshould open very suddenly when probed and havepollen released in the bud.

The large number of ancestral genera with explo-sive flowers leads to the question of whether explo-sive flowers are ancestral (shared) or have arisenindependently four or more different times. Since amajority of Loranthaceae do not have explosiveflowers, independent origin may be more likely.Loranthaceae have close relationships with birds,both for pollination and for dispersal (Reid 1991;Ladley & Kelly 1996), and the flower structure maybe such that explosive flowers are readily selectedfor. The Alepis — Peraxilla group suggests how thismay develop. If loranth flowers, like Alepis, gener-ally have most or all of their nectar present in thebud (see Table 4, and also Davidar (1983) andFeehan (1985)), then when there is competitionamong pollinators (i.e., when pollinators are abun-dant) there will be pressure for birds to get first ac-cess to the nectar by opening buds prematurely. Thepresence of fenestrae between the petals assists pre-mature opening since it allows access to the interiorof the flower. If pollen is released in the bud thispremature opening could be classified as

facultatively explosive. Once some birds open flow-ers by twisting buds or unzipping fenestrae, there canbe selection for flowers whose petals adhere togethertightly for longer, to protect the nectar from rain orto exclude nectar thieves (Ali 1931), i.e., becomeobligately explosive. This process could have oc-curred independently a number of times.

Finally, consider the distribution of one-stageversus two-stage explosive flower mechanisms(Polhill 1989). In two-stage opening, the foragingbird first grasps the bud in its bill and gently squeezesor twists. This causes the petals to explode open intoa symmetrical flower. The bird then inserts its beakinto the open flower and takes the nectar (as illus-trated by Ladley & Kelly 1995a). In one-stage open-ing, the foraging bird inserts its bill into one of thefenestrae (the splits between the petals) in the corollaof a mature bud. This causes the petals to unzip andthe flower explodes open zygomorphically. Thestigma and anthers often swing out towards the bird,enhancing the effectiveness of pollination. Twogenera {Globimetula and Moquiniella) show an in-termediate two-stage mechanism where the secondmovement produces a zygomorphic flower orientedtowards the pollinator (Polhill 1989). One-stageflower opening is apparently more advanced, and inseveral African genera flowers have extensivespecialisations for this mode of opening (Feehan1985; Polhill 1989) such as in Erianthemum dregeiin which the anthers are thrown out of the flower bythe explosion (Evans 1895). One-stage flower open-ing is more common in Africa than two-stage open-ing (Feehan 1985). The only species reported withone-stage explosive flowers outside the Africangroup with x = 9 chromosomes is the extinctTrilepidea adamsii in New Zealand (Ladley & Kelly1995a). The existence of one-stage explosive flow-ers in this ancestral species is remarkable (althoughas Trilepidea is extinct, its pollination mechanismcan only be inferred from structural cues). Sinceexplosive opening was only recently discovered inTrilepidea, there may be other one-stage explosiveflowers in the Loranthaceae which have not yet beendescribed.

Flower visitation and nectar productionschedulesAll three bird-pollinated New Zealand species pro-duced large quantities of nectar, especially thePeraxilla spp. Most overseas Loranthaceae producemuch smaller amounts and present smaller rewards(Table 4), although Muellerina eucalyptoides has alarge reward. The abundant nectar in Peraxilla


flowers may be due to the relatively large size of theNew Zealand pollinators compared with the birdswhich pollinate overseas mistletoes. Male tui weigh121 g and male bellbirds weigh 30.7 g (Craig et al.1981), compared with average weights of 5—10 g forfour common mistletoe pollinators (two sunbirds, aflowerpecker, and a white-eye) in southern India(Davidar 1984). Therefore, the New Zealand birdshave higher energetic needs and are likely to foragepreferentially on plants which produce abundantnectar. The same arguments may apply to M.eucalyptoides, which is visited by five birds (Reid1986), the largest of which is the little wattlebird at65 g (Paton & Ford 1977).

The timing of nectar production can affect thevisitation schedules of pollinators (Paton 1982). InAlepis and Peraxilla, unless flowers are forced openprematurely, little nectar is produced after the budis opened. This would encourage single-visit polli-nation systems where the birds concentrate on open-ing ripe buds, where the nectar has demonstrably notalready been harvested by another bird. Field obser-vations on Peraxilla show that this is largely whattui and bellbirds do. However, when ripe buds arerare (late in the flowering season, or if pollinatorsare abundant) the search time to find ripe buds in-creases and it may be more profitable to glean smallamounts of nectar from open flowers. If birds areabundant a fraction of flowers may also have beenopened prematurely and these will continue to se-crete nectar after opening. Both Peraxilla and Alepisflowers change colour with age after flowers havebeen opened, so birds could identify recently-openedflowers. At some sites, P. tetrapetala flowers maybe opened by pollen-harvesting bees (Kelly et al.1996), in which case open flowers with abundantnectar would be present which would also encour-age birds to forage on open flowers. Therefore, wewould expect both Peraxilla and Alepis to have lowbut non-zero levels of revisitation of open flowersby birds.

Dominance relationships between bird species arealso important. Gill & Wolf (1975) found that inPhragmanthera dshallensis larger sunbirds weremainly opening ripe buds to get nectar, whereas thesmaller species of sunbird were more often moppingup already-open flowers. In Australia, the smallerhoneyeater species visit Antyema flowers early andlate in the flowering season, while the larger, domi-nant honeyeaters concentrate on the middle of theflowering season when the number of open flowersis highest (Bernhardt & Calder 1981). In this studywe found that tui excluded other bird species,

including bellbirds, from both P. colensoi and P.tetrapetala at the Nelson sites, but not at Waiouruor on Little Barrier Island. Presumably tui defend themost valuable resource at any given time, which wasPeraxilla at Nelson (in a mixed grassland/A^or/jo-fagus forest area) but something else on Little Bar-rier (in diverse continuous native forest).

Breeding systemsIf birds visit solely or mainly buds, the flowers getvisited only once or a few times. This limits theoptions of the plant for separation of male and fe-male function. Lloyd & Webb (1986) hypothesisedthat herkogamy (separation of male and female func-tion in space) and dichogamy (separation in time)evolved to avoid interference between the two func-tions of pollen receipt and pollen dispatch. If theflowers are only visited once then dichogamy wouldnot be successful, and the flowers would be expectedto show some form of herkogamy. This is the casein Peraxilla and A.flavida. After opening there is aspatial gap between the stigma and the dehiscedanthers, and in all three species if the foraging birdenters the flower from the top it contacts the stigmabefore touching the anthers. In Alepis there is nodichogamy as the anthers dehisce in the bud and thestigma is simultaneously receptive, as shown bypollen tube growth in the bud. Peraxilla also showsanther dehiscence in the bud, but in ripe buds, onlythe distal portion of the stigma is receptive ensuringthat a spatial separation of the receptive surface andthe exposed pollen is maintained. However, withincreasing age the receptive portion spreads over theentire stigma, allowing the possibility of selfing latein the life of unopened buds shortly before budsnormally 'bottom-open'. Indeed, examination of thestyle using aniline blue staining and fluoresencemicroscopy reveals that pollen tubes are sometimesfound in very old unopened buds of both Peraxillaspecies (Robertson, Kelly, and Ladley unpubl. data).These conclusions are consistent with the relativelylow fruit set (11-22%) in bagged Peraxilla buds(Ladley & Kelly 1995a; Kelly et al. 1996).

If Peraxilla flowers are opened prematurely theymay not only lack the full complement of nectar butalso may not be easily pollinated at that time as onlya small portion of the stigma is receptive. Such flow-ers may need to be double-visited, as noted in theprevious section. On the first visit pollen may beremoved and exported; fertilisation may take placeon the second visit (dichogamy). This system intro-duces some flexibility in visitation schedule allow-ing single visit pollination when pollinators are rare


but encouraging multiple visits when pollinators areabundant enough to be prematurely opening flow-ers.

In comparison with most Australian Amyema spp.which show a trend towards strong dichogamy(Bernhardt & Calder 1981), the New Zealand spe-cies show much weaker protandry with the male andfemale phases overlapping, and both phases startingbefore buds are fully ripe and ready to be opened.Another Australian mistletoe, Nuytsia floribunda,resembles A. flavida in having no dichogamy at all(Sargent 1918). However, one Amyema species (A.quandang) shows some overlap as the stigma ap-pears to be partially receptive in the male phase(Bernhardt et al. 1980) and thus appears to occupyan intermediate position in the continuum from com-plete dichogamy (most Amyema spp.) to very slight(Peraxilla spp.) to no dichogamy (Alepis andNuytsia). Dichogamous species would be expectedto have more extended periods of nectar production(to encourage multiple visits) than species with notemporal separation of male and female function.

Outbreeding is thought to be the norm within theLoranthaceae, although self-compatibility may becommon (Barlow 1983); six of eight Amyema spe-cies tested showed full or partial self-compatibility(Bernhardt & Calder 1981; Bernhardt 1982). Workon the breeding systems of explosive flowering spe-cies elsewhere is limited to a few bagged pollinator-exclusion experiments, with varing results (Table 8).Some species (e.g., Dendrophthoe pentandra,Tapinanthus kraussianus, Erianthemum dregei) donot set seed within bags, while others (e.g.,Macrosolen cochinchinensis, Dendrophthoeneelgherrensis) do set seed and hence must be self-compatible (Evans 1895; Docters van Leeuwen1954). Self-compatibility has been shown in bothspecies of Peraxilla (Ladley & Kelly 1995a; Kellyet al. 1996), and in Alepis and Ileostylus. The floralstructure, high levels of investment in nectar produc-tion, and in Peraxilla dependence on birds for floweropening and low fruit set in bagged flowers, all sug-gest that outbreeding via birds should be commonin the New Zealand species. However, data are notyet available which would allow assessment of thelevels of autogamy, geitonogamy, and outcrossingin natural populations.

Insect-pollinated speciesIleostylus micranthus and T. antarctica were foundto be dioecious or sub-dioecious, confirming earlierwork (Menzies 1947; Smart 1952). For both /.micranthus and T. antarctica the flowers were small,

less that 5 mm in diameter, and were highly scented.These characteristics match those of the other de-scribed species of unisexual loranthaceous mistletoes(Kuijt 1969), except that /. micranthus seems to bethe only member of the family which is sub-dioecious. The T. antarctica population had a fe-male-biased sex ratio, and /. micranthus had a highernumber of female plants than male or hermaphro-dite plants. Sex ratios are commonly skewed indioecious plant species, but usually towards males(Delph 1997). However, mistletoes tend to showfemale-biased sex ratios, such as in the loranthaceousBarathranthus axanthus (Docters van Leeuwen1954). Two Viscaceae have been studied: Phora-dendron tometosum had a female bias (Nixon &Todzia 1985), while P.juniperinum was 1:1 or male-biased (Dawson et al. 1990). Delph (1997) consid-ered that the common male bias may arise fromhigher female mortality caused by higher reproduc-tive allocations, whereas the female bias in Phora-dendron may be caused by differences inphotosynthetic water use efficiency between thesexes.

Ecological implicationsFinally, we address the question of whether any ofthe New Zealand mistletoes have pollination syn-dromes which would render them vulnerable to afailure of reproduction consequent on a reduction intheir pollinating animal(s). The insect-pollinatedspecies (71 antarctica, I. micranthus) seem to giveleast grounds for concern here. While the spectrumof flower visitors has not been fully described (seeSmart 1952), there are no evident specialised mecha-nisms which would prevent introduced invertebratessuch as honey bees from effecting pollination evenif native invertebrates declined in abundance.Moreover, /. micranthus is subdioecious, and thehermaphrodite plants can autonomously set self-pollinated seed. There seem to be few grounds forconcern over pollination of these two species.

Alepis flavida is probably the least at risk of thethree bird-pollinated species. Although it has explo-sive flowers, these are facultatively explosive andcan self-open, unlike Peraxilla. This makes the flow-ers accessible to opportunist pollinators such assilvereyes or insects like native bees. Moreover,Alepis is highly self-fertile and bagged Alepis flow-ers set as much seed in the absence of pollinators aswhen hand-pollinated. Vox Alepis, levels of pollinatorvisitation probably mainly affect levels of out-crossing, rather than levels of seed production.

In contrast, Peraxilla flowers are obligately


explosive and hence highly dependent on endemicbirds. Tui and bellbirds (both endemic) were respon-sible for the vast majority of pollinator visits, al-though native silvereyes visited flowers of bothPeraxilla species, and introduced chaffinchesopened P. tetrapetala flowers at one site. O'Donnell& Dilks (1994) also reported seeing silvereyes andthe endemic kaka {Nestor meridionalis) visitingPeraxilla flowers, at sites in Westland. However, ourdata suggest that non-endemic birds are numericallyunimportant for pollination, which is exactly thesame situation as for fruit dispersal in New Zealandmistletoes (Ladley & Kelly 1996). Native bees(Hylaeus agilis) do open flowers of P. tetrapetala(but not P. colensoi) at some sites, which increasesfruit set above that in unopened buds (Kelly et al.1996). Despite this, in some areas many flowers ofboth Peraxilla species currently do not get openedby anything before abscission, and unopened flow-ers have much reduced seed set, which led Ladley& Kelly (1995a, 1995b) to suggest that pollinationcould be limiting to these species. The data in thispaper confirm that view.

Therefore, we would predict that Tupeia andIleostylus are least likely, and Peraxilla spp. mostlikely, to suffer from reduced seed set through inad-equate pollination. If problems with pollination havebeen significant over the last 150 years, then wewould predict the smallest decreases in the insect-pollinated species and the greatest declines inPeraxilla. This is borne out by distribution data (deLange et al. 1997). Tupeia and Ileostylus haveadapted most readily to human ecosystems and arerelatively widespread in lowland New Zealand, butthis may be more due to their very wide host rangesincluding many introduced plants (de Lange et al.1996) than their pollination systems. Alepis, P.colensoi, and P. tetrapetala are now very uncommonin the North Island, but de Lange et al. (1997) con-cluded that Alepis and P. colensoi were never com-mon there, whereas P. tetrapetala was previouslyabundant and widespread. Therefore, it seems thatin the North Island the decline of P. tetrapetala hasbeen more marked than of Alepis, as predicted fromits greater vulnerability to pollination failure. Therate of decline of P. colensoi is less well known. Theextinct Trilepidea adamsii also had a highly special-ised explosive pollination system, which may havecontributed to its rapid decline (Ladley & Kelly1995a). Other factors such as fruit dispersal (Ladley& Kelly 1996), habitat clearance, and herbivory bypossums (Norton 1991) seem certain to also be in-volved for all native mistletoes. While possum

control has been the main focus in the past, the con-servation of the surviving Loranthaceae will be verydifficult unless populations of tui and/or bellbirdscan be maintained to provide pollination and disper-sal services.

ACKNOWLEDGMENTS

We thank the landowners for allowing us access to theirproperties, including at Wakefield the Bashford, Gullery,and Jones families, and the Department of Conservation;Donald and Bunty Ladley for accommodation on fieldwork; the Public Good Science Fund for financial sup-port; Ashley Sparrow for help with the analysis; SandraAnderson for helpful discussions on pollination in NewZealand; and Lynda Delph, Jo Kenrick, David Norton,Nick Reid, and Ashley Sparrow for helpful comments onthe manuscript.

REFERENCES

Ali, S. A. 1931: The role of sunbirds and flower-peckersin the propagation and distribution of the tree-parasite, Loranthus longiflorus Dest., in theKonkan (W. India). Journal of the Bombay Natu-ral History Society 35: 144-149.

Ali, S. A. 1932: Flower-birds and bird-flowers in India.Journal of the Bombay Natural History Society35: 573-605.

Allan, H. H. 1961: Flora of New Zealand. Vol. I. Wel-lington, Government Printer.

Armstrong, J. A. 1979: Biotic pollination mechanisims inthe Australian flora — a review. New Zealandjournal of botany 17: 467-508.

Barlow, B. A. 1966: A revision of the Loranthaceae ofAustralia and New Zealand. Australian journal ofbotany 14: 421-499.

Barlow, B. A. 1983: Biogeography of Loranthaceae andViscaceae. In: Calder, M.; Bernhardt, P. ed. Thebiology of mistletoes. Sydney, Academic Press.Pp. 19-46.

Barlow, B. A.; Hawksworth, F. G.; Kuijt, J.; Polhill, R.M.; Weins, D. 1989: Genera of mistletoes. Goldenbough 11: \-$.

Bernhardt, P. 1982: Interspecific incompatability amongstVictorian species of Amyema (Loranthaceae).Australian journal of botany 30: 175—184.

Berndardt, P. 1983: The floral biology of Amyema insouth-eastern Australia. In: Calder, M.; Bernhardt,P. ed. The biology of mistletoes. Sydney, Aca-demic Press. Pp. 87-100.


Bernhardt, P. 1984: Mistletoes on mistletoes: the floralecology of Amyema miraculosum and its host A.miquelii. Australian journal of botany 32: 73—86.

Bernhardt, P.; Calder, D. M. 1981: The floral ecology ofsympatric populations of Amyema pendulum andAmyema quandang (Loranthaceae). Bulletin ofthe Torrey Botanical Club 108: 213-230.

Bernhardt, P.; Knox, R. B.; Calder, D. M. 1980: Floralbiology and self-incompatibility in some Austral-ian mistletoes of the genus Amyema (Loran-thaceae). Australian journal of botany 28:437-451.

Calder, D. M; Eager, R. W.; Bernhardt, P. 1979: Intro-duction to the ecology and floral biology ofAmyema (Loranthaceae) in south-east Australia.In: Musselman, L. J.; Worsham, A. D.; Eplee, R.E. ed. The second International Symposium onParasitic Weeds. Raleigh, North Carolina StateUniversity. Pp. 1-13.

Connor, H. E.; Edgar, E. 1987: Name changes in theindigenous New Zealand flora, 1960—86 andNomina Nova IV, 1983—86. New Zealand jour-nal of botany 25: 115-170.

Craig, J. L.; Stewart, A. M; Douglas, M. E. 1981: Theforaging of New Zealand honeyeaters. New Zea-land journal of zoology 8: 87—91.

Davidar, P. 1983: Similarity between flowers and fruitsin some flowerpecker pollinated mistletoes.Biotropica 15: 32-37.

Davidar, P. 1984: Ecological interactions between mis-tletoes and their avian pollinators in South India.Journal of the Bombay Natural History Society82: 45-60.

Dawson, T. E.; Ehleringer, J. R.; Marshall, J. D. 1990:Sex-ratio and reproductive variation in the mis-tletoe Phoradendron juniperinum (Viscaceae).American journal of botany 77: 584—589.

de Lange, P. J.; Norton, D. A.; Molloy, B. P. J. 1996: Arevised checklist of New Zealand mistletoe(Loranthaceae) hosts. New Zealand BotanicalSociety newsletter 44: 15-24.

de Lange, P. J.; Norton, D. A.; Molloy, B. P. J. 1997:Historical distribution of New Zealand's loran-thaceous mistletoes. In: de Lange, P. J.; Norton,D. A. ed. Ecology and conservation of New Zea-land's Loranthaceous mistletoes. Wellington,Department of Conservation. Pp. 11—22.

Delph, L. F. 1997: Sexual dimorphism in life history. In:Geber, M. A.; Dawson, T. E.; Delph, L. F. ed.Gender and sexual dimorphism in floweringplants. Berlin, Springer-Verlag.

Docters van Leeuwen, W. M. 1954: On the biology ofsome Javanese Loranthaceae and the role birdsplay in their life historic Beaufortia 4: 105—205.

Evans, M. S. 1895: The fertilisation of Loranthuskraussianus and L. dregei. Nature 51: 235—236.

Feehan, J. 1985: Explosive flower opening in ornithophily:a study of pollination mechanisms in some Cen-tral African Loranthaceae. Botanical journal ofthe Linnean Society 90: 129-144.

Ford, H. A. 1979: Interspecific competition in Australianhoneyeaters-depletion of common resources. Aus-tralian journal of ecology 4: 145—164.

Gill, F. B.; Wolf, L. L. 1975: Foraging strategies andenergetics of East African sunbirds at mistletoeflowers. American naturalist 109: 491-510.

Godley, E. J. 1979: Flower biology in New Zealand. NewZealand journal of botany 17: 441-466.

Johow, F. 1900: Zur Bestaubungsbiologie chilenischerBluten. Verhandlungen des Deutschen wissen-schaftlichen Vereins zu Santiago de Chile 4: 233—255.

Kearns, C. A.; Inouye, D. W. 1993: Techniques for polli-nation biologists. Boulder, Colorado, UniversityPress of Colorado.

Keeble, F. W. 1896: Observations on the Loranthaceae ofCeylon. Transactions of the Linnaean Society ofLondon 5: 91-119.

Kelly, D.; Ladley, J. J.; Robertson, A. W.; Edwards, J.;Smith, D. C. 1996: The birds and the bees. Nature384: 615.

Kirkup, D. W. 1984: Avian visitors to some West Africanmistletoes. Golden bough 5: 3-4.

Kuijt, J. 1969: The biology of parasitic flowering plants.Los Angeles, University of California Press.

Ladley, J. J.; Kelly, D. 1995a: Explosive New Zealandmistletoe. Nature 378: 766.

Ladley, J. J.; Kelly, D. 1995b: Mistletoes: how theseshowy specialists and honeyeaters need each other.Forest and bird 278: 16-21.

Ladley, J. J.; Kelly, D. 1996: Dispersal, germination andsurvival of New Zealand mistletoes (Loran-thaceae): dependence on birds. New Zealand jour-nal of ecology 20: 69-79.

Lloyd, D. G.; Webb, C. J. 1986: The avoidance of inter-ference between the presentation of pollen andstigmas in angiosperms. I. Dichogamy. New Zea-land journal of botany 24: 135—162.

Martin, N. J. 1983: Nuclear DNA variation in the Aus-tralasian Loranthaceae. In: Calder, M.; Bernhardt,P. ed. The biology of mistletoes. Sydney, Aca-demic Press. Pp. 277-294.

Menzies, B. P. 1947: Some observations on the parasiticspecies Loranthus micranthus (Hook). Unpub-lished M.Sc. thesis, University of Auckland, NewZealand.


Nixon, K. C , Todzia, C. A. 1985: Within-population,within-host species and within-host tree sex ra-tios in Mistletoe (Phoradendron tomentosum) incentral Texas. American Midland naturalist 114:304-310.

Norton, D. A. 1991: Trilepidea adamsii: an obituary for aspecies. Conservation biology 5: 52—57.

Noske, R. A. 1993: Brugiera hainesii: another bird-polli-nated mangrove? Biotropica 25: 481^483.

O'Donnell, C. F. J.; Dilks, P. J. 1994: Foods and foragingof forest birds in temperate rainforest. SouthWestland, New Zealand. New Zealand journal ofecology 18: 87-107.

Paton, D. C. 1982: The influence of honeyeaters on flow-ering strategies of Australian plants. In:Armstrong, J. A.; Powell, J. M.; Richards, A. J.ed. Pollination and evolution. Sydney, Royal Bo-tanical Gardens Trust. Pp. 95-108.

Paton, D. C; Ford, H. A. 1977: Pollination by birds ofnative plants in South Australia. Emu 77: 73—85.

Polhill, R. M. 1989: Speciation patterns in AfricanLoranthaceae. In: Holm-Nielsen, L. B.; Nielsen,I. C; Balslev, H. ed. Tropical forests. London,Academic Press. Pp. 221-236.

Reid, N. 1986: Pollination and seed dispersal of mistle-toes (Loranthaceae) by birds in Southern Aus-tralia. In: Ford, H. A.; Paton, D. C. ed. Thedynamic partnership. Birds and plants in South-ern Australia. Adelaide, Government Printer. Pp.64-84.

Reid, N. 1991: Coevolution of mistletoes and frugi vorousbirds? Australian journal of ecology 16: 457—469.

Sargent, O. H. 1918: Fragments of the flower biology ofWestralian Plants. Annals of botany 32:215-231.

Smart, C. 1952: The life history of Tupeia Cham, et Schl.(Loranthaceae). Transactions of The Royal Soci-ety of New Zealand 79: 459-466.

Snow, A. A.; Spira, T. P. 1991: Differential pollen tubegrowth rates and non-random fertilization in Hi-biscus moscheutos. American journal of botany78: 1419-1426.

Webb, C. J.; Sykes, W. R.; Gamock-Jones, P. J. 1988:Flora of New Zealand. Vol. IV. Christchurch,Botany Division, Department of Scientific andIndustrial Research.

Wolf, L. L.; Stiles, G.; Hainsworth, F. R. 1976: Ecologi-cal organization of a tropical highland humming-bird community. Journal of animal ecology 45:349-379.

Zeisler, M. 1938: Uber die Abgrenzung der eigentlichenNarbenflache mit Hilfe von Reaktionen. Beiheftezum Botanisches Zentralblatt A 58: 308-318.

Explosive flowering, nectar production, breeding systems, and pollinators of New Zealand mistletoes...

Documents

Transcript of Explosive flowering, nectar production, breeding systems, and pollinators of New Zealand mistletoes...