by A. V. Milewski WHY SUCCULENT FLOWERS SEJ Seeds of Kiggeluriu ufricunu The Field Guide to Trees of Southern Africa by Van Wyk & Van Wyk (Struik 1997) shows the flowers and fruits of trees and tall shrubs in the south-western Cape. Of eighty species (excluding conifers) with fleshy fruits eaten by birds, 91 % have small, dull flowers which easily escape the notice of the human observer. Members of up to thirty-nine genera in twenty-five families conform in having fly-pollinated flowers and bird-sown seeds in the south-western Cape. Eight percent (e.g. Glllysanthe- maides, Grewia, Solanum) resemble many species of cultivated fruits (e.g. apples, plums, raspberries) in having colourful petals attracting medium-size insects such as bees and beetles. The only species of tree or tall shrub in the south-western Cape that uses birds for pollination as well as seed-dispersal is Halleria lucida. However, the sunbirds that pollinate the mainly red flowers of this honey- suckle are not among the birds that usually eat its dark purple fruits. There are fifty-two species of trees and tall shrubs with dry fruits ignored by most h'uit-eating birds in the south- western Cape. A few (e.g. Dadanaea, Glutia) have the small, dull flowers otherwise associated with succulent h'uits, but most have colourful flowers (e.g. pink in Galadendrum), or small whitish flowers massed together for display (e.g. Buddleja, Brabejum, Gunania). Blooms attractive to birds are found in Proteaceae, Aloe, Burchellia, and Schatia in the south- western Cape, according to Van Wyk and Van Wyk. There are also more than sixty local species of Erica not qualifying as tall shrubs, pollinated by sunbirds. Unlike many Ericaceae found in the Mediterranean Basin' and on other continents (e.g. blueberry), these have dry fruits. Many of the common species of bulbuls, starlings, and weavers of the south-western Cape are capable of sucking nectar and pollinating flowers. Even the fruit-eating speckled mousebird and rameron pigeon have been observed taking nectar from Aloe, without destroying the petals, elsewhere in South Africa. However, most birds usually ignore nectar, and energy, water and nutrients which are not retrieved by the plant, because the very purpose of fruit-pulp is to be removed from the plant once it is ripe. The more resources the plant spends on flowers, the less generous it is likely to be with fruit-pulp. Plants may be generally faced with a choice of dispersing pollen or seeds, but not both, by avian flight. The division between bird-polli- nated and bird-sown plants is clear in the south-western Cape, which has a climate with winter rainfall and summer drought similar to the Mediterranean Basin. Proteas charac- teristic of this area produce large blooms pollinated by sun birds and sugarbirds. Olives (Oleaceae) produce succulent fruits conspicuous to mousebirds and bulbuls (lacking gizzards) and the rameron pigeon (which has a gizzard gentle on seeds, compared to seed-destroying doves and pigeons). Although proteas lack petals, and spend energy on bulky protection for their dry seeds, each bloom contains many flowers that do not produce seeds. For each seed produced, pro teas devote more energy to nectar than to fruits. Seeds of certain species of Leucaspermum and Mimetes have a small food-body attached like a handle, sufficient to reward ants for sowing the fallen seeds. HowiWer, this does not cost as much as the swee"t·or oily wrappings on the seeds of Rhus, Gymna- sparia and Putterlickia. These members of the Anacardiaceae and Celastraceae have small flowers, and are accordingly by birds although tlo1'eir frJits lose their succulence by drying out as they ripen, in the south-western Cape and elsewhere under similar climates. Two types of plants often break the rule that succulent flowers and succulent fruits tend to be mutually exclusive. Various honeysuckles may produce copious nectar in tubular flowers, followed by sweet, succulent fruits. These fast-growing shrubs act as pioneers, temporarily enjoying access to resources sufficient for plants larger than themselves. Mistletoes (Loranthaceae) may produce bird-pollinated flowers and red, succulent fruits. Because parasitic plants suck juices from trees and shrubs used as hosts, some mistletoes are able to afford nectar as well as paying small perching birds to sow sticky seeds on the stems of host plants. Honeysuckles are represented in the south-western Cape by HaIJeria (Scrophulariaceae) and at least one species of Lycium (Solanaceae). Mistletoes in this area include Septulina glauco, which parasitizes Lycium. Cape sugarbird F lowers and fTllits vary greatly in size and how much food they offer polli nators. The smallest flowers are dull greenish, and attract pollinators no larger than small flies. Large blooms usually produce enough nectar to attract birds as pollinators. Fruits vary in an inverse way to flowers. A generous succulent wrapping may be digested by birds, rewarding them for passing the seeds intact for germination. This ripe fruit- pulp may consist of up to 90% fruit- juice. Alternatively, fruits may dry and split with maturity, releasing dry seeds. What is odd is that it is usually the large, generous flowers that produce the dry fruits, and the small flowers, with negligible nectar, that produce the succulent fruits. Birds are affected accordingly. Birds with syringe-shaped beaks suck nectar while pollinating flowers, and birds with relatively stout beaks swallow fruits, extracting the juice in their stomachs before regurgitating or defaecating the whole seeds. What is odd is that bird species specializing in nectar usually do not take fruit-juice, and vice versa. This mutual exclu- siveness between flowers and fruits, expressed in both plants and birds, is so common that it has virtually been overlooked by Science. Why do succulent flowers seldom produce succulent fruits, and why do birds not accept nectar and fruit-juice in combination? Perhaps the basic reasons are that few plants can afford to produce fruit-juice after producing nectaI' and large flowers, and nectar is not rewarding enough to attI'act birds to carry items larger than pollen grains. Plants pay birds to carry their propagules, by offering fuel, usually in the form of sugars. However, there are extI'a costs. Petals are fragile, and the nutI'ients they contain may be wasted after serving their purpose of display. Although not eaten by polli- nating birds, petals may be eaten by other animals. Blooms do not sustain themselves by photosynthesis, because a green colour would hide them from biI'ds. Fruits contain 80 Veld &' Flora June 2000
Transcript
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.
