by A. V. Milewski

WHY SUCCULENT FLOWERS SEJ

Seeds of Kiggeluriu ufricunu

The Field Guide to Trees ofSouthern Africa by Van Wyk & VanWyk (Struik 1997) shows the flowersand fruits of trees and tall shrubs inthe south-western Cape. Of eightyspecies (excluding conifers) withfleshy fruits eaten by birds, 91 % havesmall, dull flowers which easilyescape the notice of the humanobserver. Members of up to thirty-ninegenera in twenty-fi ve families conformin having fly-pollinated flowers andbird-sown seeds in the south-westernCape. Eight percent (e.g. Glllysanthe­maides, Grewia, Solanum) resemblemany species of cultivated fruits(e.g. apples, plums, raspberries) inhaving colourful petals attractingmedium-size insects such as bees andbeetles. The only species of tree or tallshrub in the south-western Cape thatuses birds for pollination as well asseed-dispersal is Halleria lucida.However, the sunbirds that pollinatethe mainly red flowers of this honey­suckle are not among the birds thatusually eat its dark purple fruits.

There are fifty-two species of treesand tall shrubs with dry fruits ignoredby most h'uit-eating birds in the south­western Cape. A few (e.g. Dadanaea,Glutia) have the small, dull flowersotherwise associated with succulenth'uits, but most have colourful flowers(e.g. pink in Galadendrum), or smallwhitish flowers massed together fordisplay (e.g. Buddleja, Brabejum,Gunania). Blooms attractive to birdsare found in Proteaceae, Aloe,Burchellia, and Schatia in the south­western Cape, according to Van Wykand Van Wyk. There are also morethan sixty local species of Erica notqualifying as tall shrubs, pollinated bysunbirds. Unlike many Ericaceaefound in the Mediterranean Basin'andon other continents (e.g. blueberry),these have dry fruits.

Many of the common species ofbulbuls, starlings, and weavers of thesouth-western Cape are capable ofsucking nectar and pollinatingflowers. Even the fruit-eating speckledmousebird and rameron pigeon havebeen observed taking nectar fromAloe, without destroying the petals,elsewhere in South Africa. However,most birds usually ignore nectar, and

energy, water and nutrients which arenot retrieved by the plant, because thevery purpose of fruit-pulp is to beremoved from the plant once it isripe. The more resources the plantspends on flowers, the less generous itis likely to be with fruit-pulp. Plantsmay be generally faced with a choiceof dispersing pollen or seeds, but notboth, by avian flight.

The division between bird-polli­nated and bird-sown plants is clear inthe south-western Cape, which has aclimate with winter rainfall andsummer drought similar to theMediterranean Basin. Pro teas charac­teristic of this area produce largeblooms pollinated by sunbirds andsugarbirds. Olives (Oleaceae) producesucculent fruits conspicuous tomousebirds and bulbuls (lackinggizzards) and the rameron pigeon(which has a gizzard gentle on seeds,compared to seed-destroying dovesand pigeons). Although proteas lackpetals, and spend energy on bulkyprotection for their dry seeds, eachbloom contains many flowers that donot produce seeds. For each seedproduced, pro teas devote more energyto nectar than to fruits. Seeds ofcertain species of Leucaspermum andMimetes have a small food-bodyattached like a handle, sufficient toreward ants for sowing the fallenseeds. HowiWer, this does not cost asmuch as the swee"t·or oily wrappingson the seeds of e~. Rhus, Gymna­sparia and Putterlickia. Thesemembers of the Anacardiaceae andCelastraceae have small flowers, andare accordingly so~n by birdsalthough tlo1'eir frJits lose theirsucculence by drying out as theyripen, in the south-western Cape andelsewhere under similar climates.

Two types of plants often break therule that succulent flowers andsucculent fruits tend to be mutuallyexclusive. Various honeysuckles mayproduce copious nectar in tubularflowers, followed by sweet, succulentfruits. These fast-growing shrubs actas pioneers, temporarily enjoyingaccess to resources sufficient forplants larger than themselves.Mistletoes (Loranthaceae) mayproduce bird-pollinated flowers andred, succulent fruits. Because parasiticplants suck juices from trees andshrubs used as hosts, some mistletoesare able to afford nectar as well aspaying small perching birds to sowsticky seeds on the stems of hostplants. Honeysuckles are representedin the south-western Cape by HaIJeria(Scrophulariaceae) and at least onespecies of Lycium (Solanaceae).Mistletoes in this area includeSeptulina glauco, which parasitizesLycium.

Capesugarbird

Flowers and fTllits vary greatly insize and how much food theyoffer polli nators. The smallest

flowers are dull greenish, and attractpollinators no larger than small flies.Large blooms usually produce enoughnectar to attract birds as pollinators.Fruits vary in an inverse way toflowers. A generous succulentwrapping may be digested by birds,rewarding them for passing the seedsintact for germination. This ripe fruit­pulp may consist of up to 90% fruit­juice. Alternatively, fruits may dryand split with maturity, releasing dryseeds. What is odd is that it is usuallythe large, generous flowers thatproduce the dry fruits, and the smallflowers, with negligible nectar, thatproduce the succulent fruits.

Birds are affected accordingly.Birds with syringe-shaped beaks sucknectar while pollinating flowers, andbirds with relatively stout beaksswallow fruits, extracting the juice intheir stomachs before regurgitating ordefaecating the whole seeds. What isodd is that bird species specializing innectar usually do not take fruit-juice,and vice versa. This mutual exclu­siveness between flowers and fruits,expressed in both plants and birds, isso common that it has virtually beenoverlooked by Science.

Why do succulent flowers seldomproduce succulent fruits, and why dobirds not accept nectar and fruit-juicein combination? Perhaps the basicreasons are that few plants can affordto produce fruit-juice after producingnectaI' and large flowers, and nectar isnot rewarding enough to attI'act birdsto carry items larger than pollengrains.

Plants pay birds to carry theirpropagules, by offering fuel, usuallyin the form of sugars. However, thereare extI'a costs. Petals are fragile, andthe nutI'ients they contain may bewasted after serving their purpose ofdisplay. Although not eaten by polli­nating birds, petals may be eaten byother animals. Blooms do not sustainthemselves by photosynthesis,because a green colour would hidethem from biI'ds. Fruits contain

80 Veld &' Flora June 2000

)M PRODUCE SUCCULENT FRUITS IN MY OPINION

leave the patches of Proteaceae andErica to sunbirds and sugarbirds. Capewhi te-eyes eat both nectar and fruit­pulp, but they are too short-billed topollinate most flowers, and too smallto disperse most seeds. Instead, theycheat on both types of plants, stealingnectar by pecking holes in floral tubesto avoid the anthers, and stealingfruit-pulp by pecking holes into fruitswithout swallowing seeds. Hallerialucida can be sown even by white­eyes because its fruit-pulp containsmany small seeds. Even in the case ofmistletoes in the south-western Cape,the pollinators (sunbirds) differ fromthe seed-sowers (e.g. pied barbet).

Nectar-eating birds are everywheresmaller than fruit-eating birds,although size-ranges overlap. Thelargest pollinator (Cape sugarbird at35 g) is less than one-tenth the bodymass of the largest seed-sower in thesouth-western Cape. Indeed, therameron pigeon is more massive thanany bird specializing in nectar,including the relatively largeAustralian honeyeaters. The Capesugarbird is nearly as large as theCape bulbul, but is much smaller thanthe speckled mousebird (50 g). Thesmallest nectar-eater (lesser double­collared sunbird at 8 g) is dwarfed bythe smallest fruit-eater (sombre bulbulat 29 g) in the south-western Cape.The whole bodies of the smallesthummingbirds, found in the WestIndies, are smaller (2-3 g) than thelargest seeds sown by flying birds (aslarge as seeds of the cultivated olive).

A basic explanation for the smallsize and distinctive beak shape ofnectar-eating birds is that pollen islighter than seed, and can be carriedby even the smallest of feathers. Thelargest pollen grains are only 0.2 mm,sufficient to fertilize the seed, whereasthe seed must start a whole new plant.Plants are unlikely to pay more thannecessary for transport of theirpropagules. Pollen can be carried bysmall birds that require relativelysmall amounts of fuel. Only relativelylarge birds are likely to swallow seedsindigestible to them. The bird flieswith a considerable load until it sowsthe eed, except where certain mistletoeseeds are regurgitated within minutes.

Hence, nectartends to be aless substantialreward thanfruit-pulp.Fruit-juicecontainspotassium,unnecessaryin nectar, and

Cape white-eye

certain fruits (e.g. Kiggelaria africanain the south-western Cape) containfats as well as sugars. The availablepayment of dilute energy can sustainonly relatively small body sizes, andplants do not encourage the eating ofpetals needed for display. Fruit-eatingbirds require extra protein rather thanenergy, and are unlikely to be attractedto the meagre rewards offered byplants for the transportation of pollen.

Nectar-eating birds differ in shapefrom fruit-eating birds, mainly becauseof their sizes. The beaks and tonguesof sunbirds, sugarbirds, humming­birds, and honeyeaters are not neces­sarily longer than those of fruit-eatingbirds but are effectively syringes fittedto small bodies. Bird-pollinated

, The more resources the plantspends on flowers, the lessgenerous it is likely to be withfruit-pulp. Plants may begenerally faced with a choiceof dispersing pollen or seeds,but not both, by avian flight.,

flowers assume tube shapes accord­ingly, which may be composed intoblooms of brush form (Proteaceae).Accor~ing to the costs and rewards ofcarrying pollen from flower to flower,nectar-eating'birds can be seen asessentially'small, and consequentiallylong-beaked, birds. Hummingbirdsand sunbirds can afford to hover atflowers or chase. tiny gnats, midgesand s'piders~qecause their diet is oneof sU'perfluolls energy, relative tonutrients.

Although the supply of water andenergy depends on climate, the distri­bution and body sizes of nectar- andfruit-eating birds differs greatly amongareas with winter rainfall and summerdrought on different continents. TheMediterranean Basin has many bird­sown plants, but only one pollinatingbird (Palestine sunbird). Australia hasmany Proteaceae and eucalypts polli­nated by honeyeaters and parrots.Plants with succulent fruits areinconspicuous in Australia, yet evenEricaceae and Proteaceae have seedssown by the emu. The main trees andshrubs under winter rainfall in theAmericas produce little nectar.However, California contains honey­suckles (e.g. Hibes speciosum) andherbaceous Scrophulariaceae (e.g.hemiparasitic CastjJJeja) pollinated byhummingbirds, and Chile containsforests of Cryptocarya alba with red,succulent fruit. Even the largest ofAmerican hummingbirds (more than15 g) hovers more frequently than the

smallest of Australasian honeyeaters(less than 10 g). South Africa alonecontains certain vegetation typesdominated by bird-pollinated plants(e.g. Pratea fynbos) and othersdominated by bird-sown plants (e.g.thickets and forests of Olea). Since allthe vegetation of low trees or tallshrubs here is dominated by eitherbird-pollinated or bird-sown plants,it is remarkable that there are noequivalents for small hum.mingbirds,large honeyeaters, the Australianmistletoebird or the emu in thesouth-western Cape.

Unusually large ground orchidsattract relatively large pollinators inthe south-western Cape. Most orchidsare particularly thrifty with theirsweet juices, perhaps because theyphotosynthesize relatively slowly, andrely for energy partly on decomposingplant matter. Orchids tend to producelittle nectar, instead deceiving polli­nators by mimicry. These plants alsoprod uce aggregated pollen, which isdeposited in a cohesive mass(pollinium) on visiting pollinators.Because their wind-borne seeds arehardly larger than pollen grains,orchids are among the few plants inwhich pollen is effectively moremassive than seed. Satyrium carneum,70 em high, produces enough nectarto attract the smallest species ofsunbird in the south-western Cape. Itthus appears to be the most generouswith its juices of the hundreds ofspecies of ground orchids found undersimilar climates in the MediterraneanBasin, the Americas, and Australia.Is any bird deceived into dusting itsplumage with orchid seeds?

The fact that flower type varieslittle within each plant family allowsus to recognize families. However,flower size and generosity with nectar,and fruit texture and size, vary greatly,so that either the flowers or fruits areusually displayed in any particularspecies. Regardless of plant families,species with succulent fruits are notpollinated by birds except in the mostaffluent of situations. In view of thispredictability, the great variation inthe succulence of flowers and fruitsunder similar climates on differentcontinents is intriguing. Perhaps thekey is differences in fire regimes andthe availability of potassium.But that is another topic ... @

AcknowledgementI thank Richard Dean, Steve Johnson, SueMilton, Terry Oatley and Peter Ryan fortheir enjoyable contributions to this article.The drawings by Jeanette Loedolff arereproduced, with kind permission from theNBI, from the book Discovering indigenoLIsforests at Kirstenbosch.

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